Aquaculture 182 Ž2000. 173–182
www.elsevier.nlrlocateraqua-online
Management of Manila clam beds
I. Influence of seed size, type of substratum and
protection on initial mortality
J. Cigarrıa
´
a
a,)
, J.M. Fernandez
´
b
´ de Zoologıa,
Area
´ Departamento Biologıa
´ de Organismos y Sistemas, UniÕersida´ d’UÕieu,
Principau D’Asturies, Spain
b
CultiÕos Marinos, Paseo del Muelle sr n, 33760 Castropol, Asturias, Spain
Accepted 6 July 1999
Abstract
Commercial Manila clam beds in the Eo estuary ŽNW Spain. were studied from 1991 to 1996
to determine the influence of seed size, level of protection and substratum type on mortality early
in the culture period. We detected a significant effect of size on mortality in both protected and
unprotected beds, as, even with predator control, smaller seed showed poorer survival when
planted in the field. A significant influence of substratum on mortality was also evident, with
lowest mortality in sand–gravel beds. Clams reached a size-refuge at 1 g Ž16 mm in shell length.
when protected with nets from predators and at 2 g Ž21 mm in length. when unprotected, showing
how the net reduced the availability of clams to predators. Therefore, planting larger clams in
sand–gravel beds and protecting them with nets will enhance clam survival. q 2000 Elsevier
Science B.V. All rights reserved.
Keywords: Manila clam; Ruditapes philipinarum; Management; Survival; Seed size; Size-refuge; Substratum;
Eo estuary
1. Introduction
Efficient operation of an aquaculture business requires forecasting product availability for specific markets. Accomplishment of this objective necessitates the prediction of
future production in terms of stock growth and survival ŽRoland and Brown, 1990..
)
Corresponding author. Tel.: q34-98-510-48-39; fax: q34-98-510-48-68; e-mail:
[email protected]
0044-8486r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 0 4 4 - 8 4 8 6 Ž 9 9 . 0 0 2 5 7 - 4
174
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
There have been attempts to derive a general model to predict oyster growth and
survival Že.g., Askew, 1978; Hall, 1984; Roland and Brown, 1990.. Unfortunately, there
are no such models that can be applied specifically to clam culture.
There is abundant evidence that mortality rates are age-specific, but it seems unlikely
that in most cases age per se is the important factor; it is far more likely that
developmental stage, size and reproductive status are the factors that are functionally
related to survival ŽRoff, 1992.. Interspecifically, a strong correlation exists between
body size and survival in mammals, birds and fish ŽTable 5.1 in Roff, 1992., although
the mechanismŽs. generating these relationships is far from clear. So, size per se can be
a significant component of mortality rates, but in grow-out clam culture developmental
stage will be of no consequence. For example, bivalves such as Mya arenaria
ŽBrousseau, 1978. and Mytilus edulis ŽThompson, 1984., show high mortality as
juveniles and low mortality as adults, leading to a negative exponential survivorship
curve. They could be included into the Type 3 curve of Pearl and Miner Ž1935.:
‘‘Survivorship drops precipitously in the early stages of life until a certain age, size, or
life stage is reached, at which point the rate of decline is substantially reduced’’.
Size-dependent mortality factors Žpredation, competition or vulnerability to physical
stress. are often responsible for producing this survivorship pattern ŽArnold, 1984;
Kraeuter and Castagna, 1989; Nakaoka, 1996.. However, clam survival may be increased by planting large seed clams and protecting them from predators with plastic
netting. Common predators include the green crab Ž Carcinus maenas ., oystercatchers
Ž Haematopus ostralegus., trigger fish Ž Balistes capricus . and gilt-head bream Ž Sparus
auratus ..
The main goal of our work is to develop a mathematical model for clam production,
based on observed trends in growth and survival rates in relation to clam size. The
model would be similar to oyster models of Askew Ž1978. and Hall Ž1984.. Growth
models use the initial seed size and the temperature of each month to calculate the
monthly growth rates. To study the survival curves of clams in grow-out culture we
separated their life history into two phases. The first phase, high mortality, includes the
first 100 days after planting and, beyond 100 days, a second phase of low mortality.
Because survival is the most important factor affecting profit, it is necessary to optimize
the relationship between seed cost and seed survival, both dependent on seed size.
Consequently, we based our survival study on the relationship between seed size and
survival.
In this study we examine the high mortality phase of clam culture cycle. We report
here results of our work on mortality in the first 100 days following field planting. This
includes the effects of substratum and protection on the relationship between seed size
and initial mortality. This paper is the first of a series modelling clam culture.
2. Material and methods
2.1. Clam beds
From 1991 to 1996 all intertidal Manila clam beds of a commercial culture enterprise
in the Eo estuary ŽNW Spain. were monitored. More than 21 million seed clams were
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
175
Fig. 1. Survival curves of some Manila clam beds during grow-out culture. S, sand–gravel bed; M, mud bed;
P, protected with plastic netting; U, unprotected; Wi is the mean initial weight Žg. of the groups of clams.
planted during this study. Clam beds were planted in early Spring ŽMarch–April. at
densities of about 100–300 clamsrm2 , depending on seed size. Manila clam seed were
purchased from Spanish, French and Italian hatcheries Žrange: 0.24 to 9.09 g mean live
weight; 10.4 to 34 mm in shell length..
Clams were planted in four treatment types: clam beds planted in sand–gravel and
protected with plastic netting ŽS-P., sand–gravel and unprotected ŽS-U., mud-protected
ŽM-P. and mud-unprotected ŽM-U.. Particle size analyses of the mud and gravel–sand
substrates were performed following Buchanan and Kain Ž1971. and using the Wentwoth grade classification Žin % of dry weight fractions.: Silt and Clay Ž- 0.063 mm;
27% in mud vs. 7% in sand–gravel., Fine sand Ž0.062–0.25 mm; 51% in mud vs. 40%
in sand–gravel., Medium sand Ž0.25–0.5 mm; 18% in mud vs. 8% in sand–gravel.,
Coarse sand Ž0.5–2 mm; 2% in mud vs. 1% in sand–gravel., Granule Ž2–4 mm; 2% in
mud vs. 27% in sand–gravel. and Pebble Ž4–64 mm; 0% in mud vs. 17% in
sand–gravel.. Both substrate types were prepared prior to seed planting. This means that
algae and other organisms Že.g., crustaceans., obstructions, etc., were removed.
Table 1
Relationships between mortality to day 100 and initial seed size described by the regressions LnŽ10) M . s
aq b Ž1r6Wi .
Data from unprotected beds were pooled to obtain a common regression. Weight range indicates the range of
seed size Žg. included in the analysis.
Protection
Substratum
a
b
n
R2
P
Weight range
Net
Net
Unprotected
Unprotected
Unprotected
Sand–gravel
Mud
Sand–gravel
Mud
Common regression
2.0329
2.5153
4.2571
4.0013
4.2036
2.4435
2.5778
1.8965
1.8167
1.8844
17
5
15
4
19
0.855
0.904
0.787
0.987
0.829
- 0.001
- 0.01
- 0.001
- 0.01
- 0.001
0.36–2.05
0.63–1.96
0.46–9.09
0.6–9.09
0.46–9.09
176
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
Protected beds consisted of plastic nets 50 m long and 2 m wide to cover the seeded
plots Ž1.6 m in width., allowing the edges to be buried. Mesh size varied depending on
seed size but was always small enough to retain the seed Žnormally 5 = 5 and 7 = 7 mm,
rigidity around 37 grm2 .. Nets were brushed off in Spring and Autumn to eliminate
algae.
Fig. 2. Ža. Mortality to day 100 — mean initial weight regressions for Manila clams in beds: sand-protected
beds ŽS-P., mud-protected ŽM-P., sand-unprotected ŽS-U. and mud-unprotected ŽM-U.. Lines are the regression lines. We present transformed data of mortality to day 100 Žin percentage., to LnŽ10)mortality. and seed
size Žg., to Ž1r6Wi .. sqrtssquare root. Žb. Theoretical curves showing the relationships between mortality to
day 100 Ž%. and seed size Žg. for Manila clams in beds. Data from unprotected beds were pooled and
represented as one regression line ŽUnprotected., as no differences appeared between sand-unprotected ŽS-U.
and mud-unprotected ŽM-U. regressions Žsee Tables 1 and 2.. Data were detransformed to better display the
relationships.
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
177
2.2. Sampling
We collected bi- or tri-monthly samples to record growth and survival. The first
sample of a new clam bed was always taken after 3 months to allow bed stabilization.
The sampling method was as follows: a plastic square frame Ž0.25 m2 . was randomly
placed into the clam bed; substrate was taken out in a screen; it was sieved in sea water
through a 4-mm mesh and the number of live clams was counted to estimate survival.
The procedure was repeated 15 times for each sample to increase precision of estimating
mean survival Ž S . ŽIFREMER, 1988.. Fifty individuals were randomly selected from
each sample. Each clam was weighed ŽW . to the nearest 0.01 g using a digital balance.
Histological surveys were done twice a year to monitor for the presence of the bivalve
disease, Perkinsus sp., following the thioglycollate procedure of Ray Ž1966..
Baited crab traps Žmesh size 5 = 5 mm. were placed in clam beds during May–July
when green crab Ž C. maenas . activity is at its highest level. Carapace lengths Žanteroposterior axis. were recorded to determine the size of trapped crabs to the nearest 1 mm.
Temperature Ž8C. and salinity Ž‰. values were recorded weekly, at the high tide level
and at 1 m depth, near the clam beds.
2.3. Statistical analysis
We extrapolated mortality from the first sample, after 3 months, to the 100th day to
establish the relationship between the seed size and mortality at exactly the same day
Ž100th day..
Initial seed weight ŽWi . data were transformed Ž1r6Wi ., and mortality Ž M . data were
logarithmically transformed LnŽ10) M .. Then, both data sets were tested for normality
ŽLilliefors test, P ) 0.1. and homogeneity of sample variances ŽBartlett test, P ) 0.05..
An allometric regression equation using the least squares method was then used to
relate mortality at the 100th day Ž M . to initial seed weight ŽWi . for each treatment:
ž ( /
Ln Ž 10) M . s a q b 1 Wi
A two-way analysis of covariance ŽANCOVA. was employed to determinate the
effect of protection and substratum on mortality during the first 100 days, with initial
Table 2
Results of comparisons of regression lines of mortality to day 100 vs. initial seed weight using ANCOVA
Due to slope heterogeneity, we could not perform analysis of intercepts of the complete analysis. We made
ANCOVA for protected and unprotected beds separately, as differences between slopes in the overall
ANCOVA appeared between the protection types.
Factor
Complete analysis
Protected beds
Unprotected beds
Protection
Substrate
Protection=
Substrate
Substrate
Substrate
Slopes
Intercepts
df
F
P
df
F
1, 34
1, 34
1, 34
6.2
0.21
6.27
- 0.05
) 0.5
- 0.05
–
–
–
–
–
–
1, 18
1, 15
0.02
0.01
) 0.5
) 0.5
1, 19
1, 16
12.96
2.05
P
–
–
–
- 0.05
) 0.1
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
178
weight as covariate. For the ANCOVA, the assumption of equal slopes was first tested,
and without slope heterogeneity tests for equal intercepts Žadjusted means. were
performed.
3. Results
The relationship between survival of Manila clams vs. period of culture is shown in
Fig. 1. There was heavy mortality during Phase I Ž0–100 days. and substantially lower
mortality during Phase II Ž100 q days..
Relationships between mortality to day 100 and initial seed size were described by
four least squares regressions LnŽ10) M . s a q b Ž1r6Wi . ŽTable 1; Fig. 2a,b..
ANCOVA revealed significantly different mortality-initial seed weight regression
slopes between protection types ŽTable 2. but not between substrate types. A significant
interaction effect between substratum and protection type was also detected. As no
homogeneity of slopes was obtained, we could not test for intercepts. Then, regressions
of mortality in protected and unprotected beds were studied separately to clarify the
effect of substratum ŽTable 2.. Regression slopes of protected clam mortality were not
significantly different between substrates, but analysis of adjusted mean mortalities
revealed that they were significantly affected by substrate. Regression slopes of clam
mortality in unprotected plots were not significantly different and neither were the
adjusted mean mortalities by substrate type. We therefore considered that both sample
regressions of unprotected beds estimate the same population regression and we
calculated the common regression following Zar Ž1984..
The size of crabs Ž C. maenas . caught in baited crab traps during May–July is shown
in Fig. 3. No diseases were detected in the clam sets included in our statistical analysis.
Monthly mean values of salinity in the Eo estuary ranged from about 30–32‰.
Equivalent values for temperature ranged from 138C in winter to 188C in summer.
Fig. 3. Size structure in May–July of the green crab population, C. maenas, at Eo estuary.
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
179
4. Discussion
Planting large seed clams generally ensures greater survival according to clam
growers and researchers Žsee for example Walne, 1974; Kraeuter and Castagna, 1989;
Britton, 1991; Spencer et al., 1991, 1992; Beal et al., 1995.. Survival of clams planted in
the field is dependent on a number of variables such as water quality, pollution, seed
size, density, protection devices, etc. ŽKraeuter and Castagna, 1989.; however, predation
is a major factor limiting survival Že.g., Kraeuter and Castagna, 1989; Flimlin, 1993.. In
European clam culture, green crabs Ž C. maenas . are one of the most significant
predators. The literature of the past 25 years provides clear evidence of the economic
impact of C. maenas on shellfish prey ŽLafferty and Kuris, 1996.. Serious damage has
been caused by crabs to stocks of clams Že.g., Vilela, 1950; Ropes, 1968; Sanchez-Salazar
et al., 1987., Pacific oysters and mussels ŽDare et al., 1983.. Parache Ž1980. showed that
Manila clams of 8 mm in length were eaten by a wide size range of green crabs Ž7–65
mm carapace length.; whereas clams of 23.5 mm were eaten only by crabs larger than
55 mm. Also, unfortunately to growers, predators have a preference for smaller-sized
prey, even though they are able to consume larger prey ŽJuanes, 1992.. Parache Ž1980.
and Flimlin Ž1993. also reported that C. maenas is esentially a ‘‘seed predator’’ due to
its preference for small clams. In the Eo estuary, the size structure of the crab population
caught in traps in spring and summer ŽFig. 3. suggests that most clam losses to predation
occur in the range of 3–16 mm in clam length Žsee IFREMER, 1988, Table 1., the range
that hatcheries usually offer to growers.
Our results indicate that survival of unprotected seed is directly related to size ŽFig.
2b., and high levels of mortality of small seed are probably caused by size-selective
predation exerted by crabs Že.g., Arnold, 1984; Sanchez-Salazar et al., 1987; Peterson et
al., 1995. and other predators. Mortality is greatly reduced using nets ŽFig. 2a., although
mortality of protected clams is also related to size. It is possible that, if crab predation is
reduced Že.g., using nets., other factors Žseed quality, physiology, environment, etc..
become more significant. In this sense, cumulative mortality could be described as a
sum of partial mortalities caused by several factors, and interactions between them, with
crab predation possibly being the main factor. Then, size-dependent mortality of
protected beds Žwithout or little crab predation. could be attributed to the following
factors.
Ža. The inefficiency of protection against infaunal predators. The net on the surface is
ineffective against infaunal predators such as nemertean worms or polychaetes ŽMcDermott, 1976; Hidu and Newell, 1989; Flimlin, 1993; Marelli and Arnold, 1996., although
their importance as predators is unknown.
Žb. Size-related differences in vulnerability to physical stress or disturbance ŽNakaoka,
1996.. Large clams can cope more successfully with stressful situations because
weight-specific metabolic costs are substantially lower ŽBayne and Newell, 1983.. As
clams were stressed due to handling and shipping procedures before planting, smaller
clams would be more affected. In this sense, studies within species support the
hypothesis that large size can be a protection against environmental stress ŽRoff, 1992..
Žc. Crab predation persists due to net inefficiency. Survival increased with increasing
rigidity of the net and thick netting Ž500 grm2 . provided good protection against crabs
180
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
while lightweight nettings Ž- 30 grm2 . were less effective, according to Spencer et al.
Ž1992.. Our net Ž36 grm2 . appears adequate Žfollowing Spencer et al., 1992. to protect
clams as more rigid nets are very expensive and not easy to use in commercial culture.
A strategy of using double layers of nets or raising the net a few centimeters above the
bottom provided a cost-effective means of using cheaper lightweight nets ŽSpencer et al.,
1992..
Reduction in mortality appeared at different sizes Žthe size-refuge. in protected and
unprotected beds ŽFig. 2b., an obvious effect of net protection. In protected beds, Manila
clam seed reached a refuge at 1 g in weight Žapprox. 16 mm in length., whereas in
unprotected beds mortality declined at 2 g Žapprox. 21 mm in length.. This is in
agreement with the experimental data of Parache Ž1980., who showed that clams of 23.5
mm in length are only preyed upon by larger crabs Ž) 50 mm., which are very rare in
the Eo estuary ŽFig. 3.. Also, Thompson Ž1995. showed that Manila clams in unprotected plots did not survive to reach a shell length greater than 20.1 mm. Several authors
also reported similar reductions in predation when other species of clams achieved a
length of 16–20 mm Že.g., Walker, 1984; Peterson et al., 1995., although the prey size
refuge varies depending on the specific predator population.
We detected a significant effect of type of substratum on mortality. If clams are
protected and planted in mud they suffer higher mortality than those planted in
sand–gravel. If clams are unprotected, no significant differences appear between substratum, although it may be that significant differences were masked due to the high effect
of predation. The higher survival in sand–gravel beds is due to increased protection by
decreasing predator efficiency and greater stability of the substrate ŽArnold, 1984;
Peterson et al., 1995; Thompson, 1995.. The coarser material reduces crab access to the
bivalves, as more time and energy have to be put into digging in gravel than in mud
ŽSkilleter, 1994, but see Iribarne et al., 1995.. Also, turbid sediments are unfavourable
for juveniles, resulting in higher mortalities of smaller clams ŽLevinton and Bambach,
1969; Nakaoka, 1996..
5. Conclusion
Smaller seed are less expensive, but more vulnerable Že.g., to predation. and they
need more time to achieve commercial size. Growers, however, must determine if
enhanced survival is enough to overcome higher costs of large seed and if their seed
suppliers have large seed at good prices. It is well known that hatcheries have serious
problems producing large quantities of large seed at commercially viable prices.
Unfortunately, many other problems caused by the lack of knowledge about the biology
of the clams still remain. These include predator foraging ecology and habitat selection,
the effect of infaunal and epibenthic predators and the development of effective
protective devices. We must keep in mind that many European clam farms have failed in
the past years as a result of that lack of knowledge. Clam culture is much more
complicated than planting clams and returning a few years later to harvest them for
market. Correctly approached, clam farming can be profitable but it should be treated
like any other farming enterprise ŽOesterling, 1995..
J. Cigarrıa,
Aquaculture 182 (2000) 173–182
´ J.M. Fernandezr
´
181
Acknowledgements
We thank Dr. S. Degraer ŽUniversity of Gent, Belgium., Dr. J. Kraeuter ŽRutgers
Univ., USA., Dr. D. Marelli ŽFlorida Marine Research Institute, USA., Dr. D. Mitchell
ŽMadrona Shellfish, Canada., Dr. S. Ogilvie ŽNational Institute of Water and Atmospheric Research, New Zealand., A. Ojanguren ŽUniversity of Oviedo, Spain., Dr. P.G.
Olin ŽUniversity of California Sea Grant, USA. and Dr. G. Thorarinsdottir
´
´ ŽMarine Res.
Institute, Iceland. for critically reading an earlier draft of this manuscript.
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