Growth and survival of the Calafia mother-of-pearl oyster Pinctada mazatlanica (Hanley 1856) under...

Growth and survival of the Cala®a mother-of-pearl

oyster Pinctada mazatlanica (Hanley 1856) under

different sequences of nursery culture±late culture

at BahõÂa de La Paz, Baja California Sur, MeÂ xico

Mario Monteforte & Sandra Morales-Mulia

Grupo Ostras Perleras, Centro de Investigaciones BioloÂgicas del Noroeste, S.C. Mar Bermejo 195, Col. Playa Palo Santa

Rita. La Paz, Baja California Sur, MeÂxico

Correspondence: Dr Mario Monteforte, Grupo Ostras Perleras, Centro de Investigaciones BioloÂgicas del Noroeste, S.C. Mar Bermejo

195, Col. Playa Palo Santa Rita. La Paz, Baja California Sur, CP 23080, MeÂxico. E-mail: [email protected]

Abstract

The Cala®a mother-of-pearl oyster, Pinctada maz-

atlanica (Hanley), and the Rainbow nacre shell,

Pteria sterna (Gould), represent an important re-

source for MeÂxico because of their potential in pearl

production. The present work deals with the effect of

different sequences of nursery culture-late culture

on growth and survival of P. mazatlanica, from

September 1993 to October 1994. The collected

spat presented two main size groups: small (mean

shell height of 7 mm), and large (13 mm). They

were arranged into four experimental batches for

each size group at a constant stocking density of

40±45 juvenile pearl oysters per Nestier cage. Three

batches remained in nursery culture for 2, 4 and

6 months respectively, after which they were

transferred to late culture in rail cages. A control

group remained in nursery culture for 12 months.

Growth was evaluated monthly and compared

through ANOVA and HSD Tukey tests. In addition

to the shell height, width, depth (mm) and weight

(g), data of shell volume (height 3 width 3 depth, in

mm3) was also introduced to estimate and compare

growth among the experimental groups. Mortality

was estimated by counting the dead specimens

every month and obtaining the percentage from a

100% initial survival at the start of the experiment.

The juveniles showed different responses to the

change from nursery culture to late culture; the

level of each response varied signi®cantly among

the experimental groups at the end of the study. It

seemed that a 6-month period for nursery culture

was propitious for P. mazatlanica.

Introduction

Pearl oyster culture and pearl production are widely

recognized today as the most pro®table of all

aquaculture industries (Fassler 1991; 1995). For

years, commercial pearl culture has relied mainly

on spat collection and/or controlled extractions of

wild adults (Australia), but attention has recently

moved towards hatchery research on most of the

species used today for pearl production.

However, limited information exists concerning

the optimum conditions under which pearl oysters

grow and survive in ®eld installations. It is now

agreed that the stocking density, type of culture

system, abundance and composition of associated

species, oceanographic parameters prevailing in

different culture locations, and depth at which

culture systems are installed, could be considered

among the many important factors de®ning a

culture strategy during juvenile and adult stages,

as well as during pearl formation (Gervis & Sims

1992; Monteforte 1996; Taylor, Rose, Southgate &

Taylor 1997a; Taylor, Southgate & Rose 1997b;

Taylor, Southgate & Rose 1998). The effects of these

factors are clearly expressed on growth rate, shell

shape, survival and pearl quality; these variables

have strong in¯uence in the expected results of a

# 2000 Blackwell Science Ltd 901

Aquaculture Research, 2000, 31, 901±915

culturing operation (Monteforte, Bervera & Morales

1994; Monteforte 1995; 1996). While the subject

has been extensively studied on many bivalves, such

as Pectinidae and Ostreidae, and a long list of

publications is available, for pearl oysters most of

this kind of research concentrates on Pinctada

maxima (Jameson) (Taylor et al. 1997a,b; Taylor

et al. 1998) and Pinctada fucata (Gould) (Chellam

1978; Chellam, Dharmaraj & Victor 1987; Chellam,

Velayudhan & Victor 1987). In Pinctada margariti-

fera (Linnaeus) and Pinctada martensii (Dunker) the

outgrowing culture techniques are generally exam-

ined just to the level of technical descriptions (Wada

1973; Coeroli, de Gaillande, Landret & Coatanea

1984; Gervis & Sims 1992), whereas for Pteria

penguin there is almost no information available

(Gervis & Sims 1992; Shirai 1994; Smitasiri,

Kajitwiwat & Tantichodok 1994; Beer 1999).

In BahõÂa de La Paz, Baja California Sur, MeÂxico, a

research programme for the cultivation and pearl

induction of the Cala®a mother-of-pearl, Pinctada

mazatlanica (Hanley), and the Rainbow nacre shell,

Pteria sterna (Gould), was started at the Centro de

Investigaciones BioloÂgicas del Noroeste (CIBNOR) in

1986. This paper analyses the results of a 13-month

experiment carried out between September 1993

and October 1994; growth and survival of P.

mazatlanica juveniles were evaluated during nursery

culture stages of different duration and monitored

further during late culture. To our knowledge, this

aspect has not been studied in any other Bivalve

species under experimental or commercial culture,

in spite of its evident importance on the response of

juveniles during subsequent culturing stages.

Materials and Methods

Experimental design

The present work was developed at the station El

Merito in BahõÂa de La Paz (see Monteforte & CarinÄ o

1992 for detailed description of this site). The

culture installation consists of a submarine platform

built with 1¢ and 2¢ galvanized pipes that form a

6 3 6 m horizontal frame held about 2.5 m high

over the sand bottom. Several modules of plastic

Nestier cages (0.6 3 0.6 3 0.15 m) for nursery

culture were suspended under this frame with

vertical ropes of 0.7±1.0 m length. For late culture,

`rail' cages (1.0 3 0.5 3 0.15 m, divided inside by

20 shelves or rows 5 cm wide) were used. The cages

were manufactured with rigid plastic 1.5 cm mesh

and placed over iron rod platforms, these were

anchored on the sandy bottom at 45±50 cm high.

(Fig. 1). The Nestier cages were suspended at about

11 m depth, while the rail cages were placed at

12 m depth in the same area.

The juveniles of P. mazatlanica used in this

work proceeded from generation Pmaz-GAV/93-2

(second spat collecting session of July±September

1993 at station Gaviota Island, BahõÂa de La Paz).

Collectors remained in immersion for 75 days

(Monteforte & GarcõÂa-Gasca 1994).

The sequence of nursery culture±late culture in

the present study was monitored monthly for

13 months, from September 1993 (initial t0

measurement) to October 1994 (t13). Four coded

groups were formed; three of the groups underwent

2, 4 and 6 months of nursery culture respectively

Figure 1 Diagram of the rail

cages used for late culture of

P. mazatlanica in the present work.

902 # 2000 Blackwell Science Ltd, Aquaculture Research, 31, 901±915

Pinctada mazatlanica culture M Monteforte & S Morales-Mulia Aquaculture Research, 2000, 31, 901±915

(2M, 4M and 6M), after which they were transferred

to late culture systems. An additional control group

(CM) remained in the nursery culture stage during

the whole experiment.

Immediately after harvest, an initial measure-

ment (shell height in mm) was performed on a

sample of 3500 spat from a total of about 7000 that

were recovered alive from the collectors. A non-

parametric Kolmogorov±Smirnov test for normality

was applied on the data (CSS Statistica Version 5.1

1994; Zar 1999). The test revealed a bimodal size-

frequency distribution (D = 0.1183; P < 0.01). Two

size groups were present: small juveniles (mean

shell height of 7.2 6 3.5 mm), and large juveniles

(13.0 6 3.3 mm) (Fig. 2); therefore, aside from the

codes de®ning the duration of the nursery culture

stage, `S' and `L' were assigned to distinguish small

and large size groups respectively.

All batches were placed at a stocking density of

40±45 juvenile pearl oysters in each Nestier cage

(132±148 ind./m2). This value was chosen after

previous experiences (DõÂaz-GarceÂs 1972; Singh,

BojoÂrquez & Meza 1982; Monteforte & LoÂpez

1990; Bervera 1994; Monteforte et al. 1994). Each

experimental group had two replications; further-

more, three additional Nestier cages for each group

were reserved, these contained individuals that

would be used to replace the dead juveniles in the

main experiment and its corresponding replications.

These batches were cultivated under the same

conditions as those of the main experiment; growth

and survival were also recorded. The purpose of this

strategy was to maintain a constant density in the

main experimental groups and its corresponding

replications throughout the nursery culture stage,

thus eliminating the possible in¯uence that a

decrease in stocking density, provoked by mortality,

could have on the growth trend of the batches

under study. Every replacement was carried out in

such a manner as not to alter the monthly average

size of a particular group receiving it (i.e. to replace

dead oysters in 2M group ± main and replications ±

only the reserves corresponding to this group were

used). It is important to mention that for some cases

in which a high mortality was registered, the

replications had to be used to replace the main

experimental groups when the reserves were

exhausted; fortunately this event happened rarely

and during the ®rst months of the experiment only.

When each group had accomplished a particular

nursery culture stage, the pearl oysters were

transferred to the `rail' cages for the subsequent

period of late culture (except the control groups

CMS and CML). This stage was started with 200

pearl oysters per cage, or 10 individuals per row

(400 ind./m2); as the pearl oysters increased in size

the density was gradually changed until there were

®ve or six individuals per row (100±120 pearl

oysters per cage, or 200±240 ind./m2). Usually, this

density is further decreased to 60±70 pearl oysters

per cage during the following months until speci-

mens attain 24 months (age at which pearl

induction is performed); this period is not included

in the present work. Because the mortality was very

low after the transfer to late culture, no replacement

of dead pearl oysters was realized during this stage.

Data treatment

The data of the previous sampling used to separate

the size groups of P. mazatlanica were introduced

into a `Box-and-Whiskers' exploratory analysis

Figure 2 Size-frequency distribution

of shell height (mm) in P. maz-

atlanica for a sample from the total

harvest and data obtained with the

Kolmogorov±Smirnov test for

normality. The dotted line is the

expected normal calculated by the

test.

# 2000 Blackwell Science Ltd, Aquaculture Research, 31, 901±915 903

Aquaculture Research, 2000, 31, 901±915 Pinctada mazatlanica culture M Monteforte & S Morales-Mulia

(STSC Statgraphics Version 5.0. 1991). The plot

de®nes the median of the values and encloses the

middle 50%, allowing the identi®cation of the data

range and the outlier points (smaller and larger sizes

beyond the `Whiskers'). These outilers were separ-

ated from the main group through sieving the

harvest. After this procedure, 1080 small and an

equal amount of large individuals were selected at

random. The pearl oysters of each size group were

divided into four batches of 270 individuals: main

experimental groups with two corresponding replic-

ations, each of 40±45 individuals, plus three Nestier

cages with the same stocking density for replace-

ments of each experimental group. Before starting

the experiment, several consecutive measurements

were taken and an ANOVA test was applied to the

sequential data. When a particular ANOVA yielded

signi®cant differences in average size among the

batches, the specimens were recombined and a new

sampling sequence was carried out until non-

signi®cant differences were detected. The purpose

of this strategy was to start the study with average

sizes as similar as possible among all groups, hence

to minimize the differences that could arise during

growth.

Monthly counts of dead and live pearl oysters, as

well as records of shell height, shell width and shell

depth (mm) and wet weight (g) were performed on

the main groups, its replications and reserves. These

data were taken monthly on 50% of the total live

individuals of each sample. Weight was not

recorded at the start of the experiment (September

1993), neither in the dead specimens of the

following months.

The monthly mortality was calculated as a

percentage (total initial number of pearl oysters at

t0/total number of dead at tn 3 100). The shell

dimensions of dead pearl oysters (excluding weight)

were compared with the records of average size of

alive pearl oysters in order to determine the size/age

at which death took place, and to infer whether this

occurred immediately after measuring and cleaning

or later in the month. Calculations for mortality

were performed by gathering the samples of the

main experiment and its replications only (the

reserve Nestier cages were not included).

In the present work, growth was evaluated with

ANOVA and HSD Tukey tests for some particular

months (CSS Statistica Version 5.1 1994; Zar

1999). At the end of this study (October 1994),

®nal measurements were taken on all the groups to

test for differences in size and evaluate the culture

treatments through combined ANOVA and HSD

Tukey tests.

Results

Main environmental parameters

Except for minor differences, the temporal variation

patterns of temperature and salinity that were

registered during the present study could be

considered as typical for BahõÂa de La Paz (Pearl

Oysters Research Group-CIBNOR, environmental

database 1989±99). The temperature at 10 m depth

had a maximum of 29 °C in October 1993 and

1994 and a minimum of 21 °C in February 1994

(Fig. 3). Nevertheless, the temperature in May 1994

Figure 3 Temperature (°C) and

salinity (½) in station El Merito,

BahõÂa de La Paz, between Septembre

1993 and October 1994.



(22.5 °C) was lower than in other years, the average

being usually about 23±23.5 °C. As a possible

consequence, the increase in water temperature

was slower between May and July (from 22.5 to

23 °C), whereas in other years it was quite common

to reach 24±24.5 °C in July at the same depth and

site.

The salinity, measured with a portable refracto-

meter (Aquafauna ATC), remained stable between

35½ and 37½. However, the ranges of minima

and maxima registered during the present work

(33½ in October 1993 and 38½ in May 1994

respectively), could be considered as extreme values

(Fig. 3). The minimum of 33½ was associated with

heavy rain that happened 2 days before the reading

was taken, whereas the maximum of 38½ may

have been an instrument malfunction, because it is

the highest salinity ever recorded during our

research programme.

Growth

Small-sized P. mazatlanica

Despite the consecutive combinations of juvenile

pearl oysters, a portion of individuals having smaller

shell depth always remained in one or another of

the experimental groups, giving signi®cant differ-

ences in this dimension. Finally, most of these

juveniles remained in the 6MS group (Table 1A)

Signi®cant differences in shell depth among groups

were therefore detected using the ANOVA test

(P = 0.009), but these differences were present only

between 6MS and CMS, as shown later by the Tukey

test (P = 0.004). The ANOVA test did not detect

signi®cant differences among groups in the other

dimensions (Table 1A). Therefore, it can be con-

sidered that the initial size of small-sized experi-

mental groups was acceptably similar.

In January 1994 (the last month in nursery

culture of 4MS whereas 2MS already had 2 months

in late culture), the gain in shell dimensions was

considerable in all groups. Two situations were

distinguished: (1) the ANOVA test did not indicate

signi®cant differences in shell depth among groups

(Table 1A); and (2) signi®cant differences among

the experimental groups were noted in the other

dimensions (Table 1A). However, these differences

were distributed heterogeneously, as shown later by

the Tukey test that was applied on each dimension

(Table 1B for shell volume): the CMS group seemed

to be signi®cantly larger in most of its shell

dimensions (height, width and volume) than 2MS

and 4MS but not in comparison with 6MS. Group

4MS had less weight than the others but the

difference was signi®cant only in comparison with

6MS, which contained the heaviest individuals

(Table 1A). Concerning the mass, the ANOVA test

detected signi®cant differences among the groups as

shown in Table 1A (P = 0.042), but the P-level was

so low that the HSD Tukey test was not sensible

enough as to note any of them.

March 1994 was the last month in the nursery

culture of the 6MS group. Groups 2MS and 4MS

had spent 4 months and 2 months in late culture

respectively. Signi®cant differences were detected in

all shell dimensions among the experimental groups

(Table 1A). The Tukey test showed that groups 2MS

and 4MS were signi®cantly smaller in all dimen-

sions than 6MS and CMS. No differences between

2MS and 4MS were indicated by the Tukey test in

any dimension; the same test gave non-signi®cant

values between 6MS and CMS. (Table 1B for shell

volume).

Final measurements were taken in October 1994

(Fig. 4). All the experimental groups (except CMS)

had been moved to the late culture stage for several

months. The ANOVA test detected signi®cant differ-

ences in all shell dimensions among the groups

(Table 1A). In this month, the 6MS group contained

the largest individuals. The Tukey test reported

signi®cant differences favouring this group in all its

dimensions in comparison with 2MS, 4MS and

CMS. Among these last three groups, the differences

in shell dimensions were non-signi®cant in all cases

(Table 1B for shell volume). However, considering

the volume and the mass, the CMS group was the

largest followed by 2MS and ®nally by 4MS, but it

was noted that the individuals in the CMS group

presented the smallest shell depth. (Fig. 4). Besides,

their shells had a fragile appearance and the growth

processus (marginal spines) were brittle or absent.

Large-sized P. mazatlanica

After the sequential ANOVA tests that were applied

on many recombinations, it became evident that a

homogeneous size distribution of large-sized P.

mazatlanica juveniles among the experimental

groups and their corresponding replication and

reserves would be extremely dif®cult to attain

because the alometrie was probably already affect-

ing the shell shape (Saucedo & Monteforte 1997;

Saucedo, Monteforte & Blanc 1998). To avoid

further manipulations of the individuals, the com-

binations were stopped when `the best one' was



achieved, that is, when non-signi®cant differences

were detected among 2ML, 4ML and CML, but

smaller individuals remained in the 6ML group. As

expected, the ANOVA test gave signi®cant differences

in all the initial shell dimensions (Table 2A), and the

Tukey test con®rmed that 6ML contained the

smallest individuals (Table 2B for shell volume).

In January 1994, the ANOVA test was still

detecting signi®cant differences in all shell dimen-

sions but the P-level was less than at the start in

September 1993, especially in shell width and depth

(Table 2 A). Considering the shell volume, the Tukey

test showed that the 6ML group was still signi®c-

antly smaller than 4ML and CML, but not in

comparison with 2ML (Table 2B). Taking into

account the weight and the mass, the ANOVA test

did not indicate signi®cant differences among the

groups (Table 2A).

In March 1994, once more the ANOVA test showed

signi®cant differences in shell dimensions except

Table 1 Shell dimensions and statistical calculations at some key months for the small-sized experimental groups of

P. mazatlanica during the process of nursery culture-late culture

(A) Results of the ANOVA test

Dimension® Height Width Depth Volume Weight Mass

Months Groups¯ (mm) (mm) (mm) (mm3) (g) (gr/mm3)

September 1993 2MS 7.78 9.08 1.72 123.68

4MS 7.93 9.15 1.73 131.24

6MS 7.33 8.65 1.61 110.13

CMS 7.78 8.60 1.78 121.83

ANOVA P 0.124 0.109 0.009 (*) 0.215

January 1994 2MS 23.53 24.63 5.81 3417.17 1.76 6123.22

4MS 24.14 24.81 5.64 3439.95 1.70 5992.10

6MS 24.89 25.37 5.80 3739.48 2.23 9449.06

CMS 25.74 26.40 6.06 4297.73 2.00 8536.42

ANOVA P 0.002 (*) 0.022 (*) 0.077 0.002 (*) 0.027 (*) 0.042 (*)

March 1994 2MS 27.53 28.63 7.22 5923.40 3.38 19720.98

4MS 27.19 28.24 7.00 5490.31 3.73 22278.58

6MS 31.74 32.46 7.80 8205.90 4.08 29998.81

CMS 31.71 32.50 7.78 8326.44 4.27 33776.08

ANOVA P 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*) 0.021 (*) 0.011 (*)

October 1994 2MS 46.94 45.48 12.77 28030.84 15.82 482972.20

4MS 46.44 46.67 13.03 28945.94 17.81 562336.40

6MS 52.69 53.49 14.09 40521.22 24.90 1082587.00

CMS 49.16 47.80 12.64 30439.13 19.23 711764.90

ANOVA P 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*)

(B) Results of the HSD Tukey test for shell volume

Months Groups 2MS 4MS 6MS

January 1994 MS 0.999748

6MS 0.589271 0.646

CMS 0.003 (*) 0.004 (*) 0.129

March 1994 4MS 0.835

6MS 0.000 (*) 0.000 (*)

CMS 0.000 (*) 0.000 (*) 0.996

October 1994 4MS 0.972

6MS 0.000 (*) 0.000 (*)

CMS 0.658 0.892 0.000 (*)

(*) denotes signi®cant differences.



in depth and volume (Table 2A). The Tukey

test showed somewhat heterogeneous results. In

general, it was observed that the CML group tended

to be the smallest in height and width, whereas 6ML

was apparently smaller in weight and mass. It is

interesting to note that, after 6 months of culture,

there was no clear pattern of noticeably larger or

smaller experimental groups among the large-sized

P. mazatlanica.

Finally, in October 1994 with all the groups

(except the CML) in the late culture stage, the last

measurements were taken (Fig. 5). The ANOVA test

detected signi®cant differences in all shell dimen-

sions (Table 2A). The Tukey test clearly showed that

the 6ML group contained the largest individuals

while the others tended to have similar sizes

(Table 2A and B and Fig. 5). Considering the shell

volume, the 6ML group was the largest, followed by

4ML then 2ML and ®nally CML (Table 2A and B and

Fig. 5). However, there were no signi®cant differ-

ences between 4ML with 6ML, and between 4ML

with 2ML (Table 2B). On the contrary, the CML

group was signi®cantly smaller than the rest in all

shell dimensions (Table 2A and B and Fig. 5).

Similarly, as in small-sized P. mazatlanica, the

individuals in the CML group also appeared to have

fragile shells.

Survival and mortality

Both the small- and large-sized experimental groups

suffered mortality between 20% and 50% during

the ®rst month of nursery culture (Table 3 and

Fig. 6A and B). The highest initial mortality was

found in the 6MS group with 47.5% and the lowest

in 2ML and 4MS with 20% and 22.5% respectively.

In the other groups, the mortality was about 30%

during this month (Table 3).

During the following months, the monthly

mortality did not go above 5%, except in January

1994 when the 2MS had 13.8% (Table 3). In

general, it was observed that the evolution of

Figure 4 Shell measurements and basic statistics (height, width, depth, weight, volume and mass) of small-sized P.

mazatlanica experimental groups at the end of the study (October 1994).



mortality from October 1993 (®rst record) to

October 1994 (last record) was higher in the CML

group, from 33.8% to 77.6% (43.8%), while in the

6MS, 2ML and 6ML groups this substraction gave

16.2%, 15.1% and 16.2% respectively. In the

remaining groups, this result was between 20.1%

and 23.7%. However, all groups had a rather high

total mortality, from the highest of 77.6% for CML

to the lowest of 35.1% for 2ML (Table 3).

Nevertheless, survival remained stable from the

time at which each experimental group was

transferred to late culture. The values of mortality

registered the ®rst month after each group was

moved to this stage varied between 0% and 5%;

monthly survival thereafter was 100% (Table 3 and

Fig. 6A and B). In October 1994, an increase in

mortality was observed, especially in the CMS, 4ML

and CML groups (12.5% for the ®rst two and 35%

Table 2 Shell dimensions and statistical calculations at some key months for the large-sized experimental groups of P.

mazatlanica during the process of nursery culture-late culture

(A) Results of the ANOVA test

Dimension® Height Width Depth Volume Weight Mass

Months Groups¯ (mm) (mm) (mm) (mm3) (g) (gr/mm3)

September 1993 2ML 13.67 14.77 2.83 584.46

4ML 13.67 14.37 2.76 577.89

6ML 12.00 13.49 2.35 391.79

CML 13.30 14.42 2.84 557.63

ANOVA P 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*)

January 1994 2ML 29.42 31.37 7.23 7009.09 3.40 24627.40

4ML 30.76 32.09 7.38 7742.61 3.69 29802.56

6ML 28.57 30.21 6.79 6036.68 3.13 18840.63

CML 31.12 32.81 7.37 7777.42 4.11 35751.50

ANOVA P 0.005 (*) 0.045 (*) 0.048 (*) 0.014 (*) 0.093 0.086

March 1994 2ML 34.63 36.88 9.17 12062.85 7.95 107722.70

4ML 33.77 35.81 8.92 11508.37 6.40 73638.91

6ML 34.71 36.40 8.60 11124.23 5.86 66053.18

CML 36.79 38.87 8.99 13232.72 7.69 109359.80

ANOVA P 0.005 (*) 0.021 (*) 0.208 0.122 0.003 (*) 0.028 (*)

October 1994 2ML 50.31 49.80 13.82 36013.10 21.21 947826.10

4ML 52.16 52.52 14.29 40330.48 25.07 1045758.00

6ML 54.44 54.81 14.76 45158.07 29.23 1524269.00

CML 48.57 47.17 12.41 28957.75 15.82 509337.40

ANOVA P 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*) 0.000 (*)

(B) Results of the HSD Tukey test for shell volume

Months Groups 2ML 4ML 6ML

September 1993 4ML 0.999

6ML 0.000 (*) 0.000 (*)

CML 0.936 0.971 0.001 (*)

January 1994 4ML 0.622

6ML 0.378 0.026 (*)

CML 0.585 1.000 0.022 (*)

October 1994 4ML 0.352

6ML 0.003 (*) 0.253

CML 0.036 (*) 0.000 (*) 0.000 (*)

(*) denotes signi®cant differences.



for the latter). In all three cases, the shells

(especially in the dead individuals) were thin and

had a fragile appearance; the growth processus

(marginal spines) were short and brittle or were less

frequent. Moreover, many individuals had lost their

byssus and/or took longer to close their valves as a

slow response to handling. On the contrary, the

individuals in the other groups were apparently

healthy.

This mortality in October 1994 seemed to be

related to the increase in the water temperature

(Fig. 6A and B), but with the purpose of ®nding an

additional explanation for the monthly mortality,

the temporal relationship between the monthly

average size of the dead and the alive pearl oysters

was analysed. Figure 7A and B show the average

shell height of dead individuals in comparison with

the live pearl oysters in the 6MS and 6ML groups

respectively. In practically all the cases, it was

observed that the size of dead pearl oysters in a

particular month was similar to the size of live pearl

oysters of the previous month. The pattern was alike

in the other experimental groups; this seems to

indicate that death may have taken place shortly

after the manipulations of measuring and cleaning.

Discussion

Nursery culture could be considered a critical stage

in the culture process of P. mazatlanica. The change

in living conditions, from the semi-closed environ-

ment offered by a spat collector (Monteforte &

GarcõÂa-Gasca 1994) to the `exposed' cages or boxes

used to rear the spat, represents a considerable

stress factor with which juveniles are confronted.

Handling, predation, stocking density, colonization

of associated species, etc. are just some of the

numerous additional factors affecting growth and

survival of the young pearl oysters during early

rearing (Gervis & Sims 1992; Monteforte et al. 1994;

Monteforte, Aldana, Bervera, PeÂrez, RamõÂrez,

Saucedo & Wright 1996; Taylor et al. 1998).

Figure 5 Shell measurements and basis statistics (height, width, depth, weight, volume and mass) of large-sized P.

mazatlanica experimental groups at the end of the study (October 1994).



In the commercial cultivation of most species of

Pinctada, the nursery culture is not a distinct stage

within the whole culture process. Usually, spat

remain in the collectors for as long as 6 months

after which they are removed and placed into

different kinds of rearing containers where the

culture process takes place until the time of pearl

induction operations (Wada 1973; Coeroli et al.

1984; Gervis & Sims 1992). However, for P.

mazatlanica, as well as for P. sterna, earlier works

have demonstrated that collectors must be

recovered no later than 3 months after immersion,

otherwise high mortality of spat can arise as a result

of predation and competition with associated species

(Monteforte & GarcõÂa-Gasca 1994; Monteforte &

Wright 1994; Monteforte, Kappelman & Espinoza

1995; Wright 1997). Because the harvested spat is

still small and fragile, the nursery culture consti-

tutes a well-de®ned stage in the culture process of

our local pearl oyster species. The need to introduce

a nursery culture stage had been underlined since

the early twentieth century by Don Gaston Vives,

during the ®rst world-wide commercial culture

experience of a pearl oyster species (P. mazatlanica)

in his enterprise, the `CompanÄ õÂa Criadora de Concha

y Perla de Baja California, S.A.' (1903±14) (Vives

1908; CarinÄ o & Monteforte 1995; 1999; CarinÄ o

1998).

In the present work, growth and survival of the

Cala®a mother-of-pearl oyster, P. mazatlanica, was

evaluated as a function of different nursery culture-

late culture sequences. The main hypothesis to test

was that the change of culture system at a certain

age would favour the development of juveniles to

young adults, enhancing both growth and survival.

Besides the change of culture artifact, two addi-

tional modi®cations were implicated in this transfer:

(1) the position of the individuals was moved from

horizontal to vertical; and (2) the stocking density

was increased from 132 to 148 ind./m2 in nursery

culture, to 333 ind./m2 at the start of late culture

and then was decreased again to 166±200 ind./m2

at the end of the present study.

The possible effect of the ®rst modi®cation

(change of position) could be explained by consider-

ing the normal position in which wild P. mazatlanica

live on the natural substrate. Wild individuals are

rarely observed in a horizontal position (dorso±

ventral axis related to the substrate plain). Except

when they are detached by some external factor (i.e.

a predator), their angular range lies between 35°and 145°, approximately (Monteforte & CarinÄ o

1992). It was thought that by reproducing the

same conditions during late culture the individuals

would develop more naturally and that therefore a

better growth and survival would be achieved.

Regarding the second modi®cation (stocking

density), it is well known that growth is density

dependent for many species of bivalves and it has

considerable in¯uence on survival. This has been

demonstrated, among others, on Pectinidae

(Orenzans, Parma & Iribarne 1991; Parsons &

Dadswell 1992; HernaÂndez-Llamas & GoÂmez-

MunÄ oz 1996) and Pteriidae (Coeroli et al. 1984;

Gervis & Sims 1992; Southgate & Beer 1996;

Taylor et al. 1997a). Although reduced stocking

densities may favour growth and survival of pearl

oysters (Southgate & Beer 1996; Taylor et al.

Small size Large size

Groups®Months¯ 2MS 4MS 6MS CMS 2ML 4ML 6ML CML

September 1993

October 32.5 22.5 47.5 32.5 20.0 26.3 30.0 33.8

November 1.3 6.3 3.8 5.0 0.0 6.3 6.3 5.0

December 2.5 6.3 1.3 1.3 5.0 1.3 3.8 0.0

January 1994 13.8 1.3 2.3 2.5 1.3 1.3 2.3 1.3

February 0.0 5.0 5.0 0.0 1.3 0.0 1.3 2.5

March 0.0 2.3 1.3 0.0 0.0 0.0 0.0 0.0

April ± 0.0 0.0 0.0 ± 0.0 0.0 0.0

May ± 0.0 0.0 0.0 ± 0.0 0.0 0.0

June ± ± 0.0 0.0 ± ± 0.0 0.0

July ± ± 0.0 0.0 ± ± 0.0 0.0

October 2.5 2.5 2.5 12.5 7.5 12.5 2.5 35.0

Total 52.6 46.2 63.7 53.8 35.1 47.7 46.2 77.6

Table 3 Monthly mortality (%) of

small and large-sized experimental

groups of P. mazatlanica during the

process of nursery culture-late

culture



1997a), there seems to exist a limit under which

growth of juveniles become slower and survival is

not enhanced. For P. mazatlanica, Bervera (1994)

and Monteforte et al. (1994) demonstrated that

stocking densities lower than 40 juveniles per cage

were not adequate during nursery culture in Nestier

cages.

The effect of different stocking densities on the

growth and survival of P. mazatlanica was not

evaluated in the present work. However, this

variable changed when juveniles were moved

from a constant 132±148 ind. m±2 in nursery

culture (40±45 individuals per Nestier cage), to

400 ind. m±2 at the transfer to late culture, and then

gradually to 200±240 ind. m±2 towards the end of

the study.

The results of the present work did not show a

substantial increase in size, or a signi®cant differ-

Figure 6 Plot of cumulative mortality (%) and water temperature (°C) at 10 m depth in station El Merito, BahõÂa de La

Paz, during the process of nursery culture±late culture of P. mazatlanica. A, small-sized experimental groups. B, large-

sized experimental groups.



ence among groups, the month after each batch

was transferred from nursery culture to late culture.

The effects on growth were perceptible later in the

culture process: the transfer indeed affected the

growth response of a particular group, but this

response varied among them, depending on how

long the pearl oysters had been held in the nursery

culture stage. Smaller individuals responded more

dynamically to the transfer, because the differences

in size were more rapidly noted than in larger

individuals. It was observed that the transfer to late

culture after 2 and 4 months of nursery culture

(2MS, 2ML, 4MS and 4ML), and the permanence in

this stage (CMS and CML), did not appear to be a

good strategy for enhancing growth of P. mazatla-

nica juveniles. On the contrary, 6 months in the

nursery culture seemed to be more convenient, as

the 6MS and 6ML groups grew signi®cantly faster

than the other groups. Although both groups

contained smaller specimens at the start of the

experiment, they `caught up' and even surpassed

the rest of the groups at the end of the study

(Tables 1A and B, 2A and B and Figs 4 and 5).

On the other hand, the transfer from nursery

culture to late culture did not display signi®cant

advantages for the survival of P. mazatlanica

juveniles. All groups presented high mortality the

®rst month after spat harvest, then it slowed down

during the culture with frequent monthly zeros,

regardless of the length of the nursery culture stage.

In general, the monthly mortality showed a

decrease more or less in the same months and at

the same size/age. For all groups, the decrease and

increase in the monthly mortality coincided with

colder and warmer months respectively (Fig. 6A and

B). However, higher mortality was registered in two

Figure 7 Comparison of the

monthly shell height average (mm)

between dead and live juveniles of

P. mazatlanica during the process of

nursery culture±late culture. These

®gures show the behaviour of the

experimental groups 6MS (a) and

6ML (b) as a representative scheme

of the other experimental groups.



cases: the small-sized experimental groups (in

global), and in the CML group. (Table 3 and

Fig. 6A and B).

Based on these results, it would be adventurous to

assume that a change of culturing conditions from

nursery culture to late culture actually enhanced

survival of P. mazatlanica, because another factor

apparently played an important role in the

mortality. This was the manipulation of specimens

during the initial recombinations and later while

measuring and cleaning: severing byssal attach-

ment, brushing of the shell and exposure to air are

well-known stress factors that affect survival

(Taylor et al. 1997b); probably the smaller pearl

oysters were more vulnerable, as shown by the

results (Fig. 7A and B).

Nevertheless, a 6-month period of nursery culture

for P. mazatlanica seemed to be adequate for growth

enhancement (Figs 4 and 5), although the advant-

ages for survival were not evident in this work

because of the experimental method that was

followed. It is probable that less frequent and more

careful manipulations (i.e. every 2 months, no

recombinations, no byssus severing, etc.) of the

pearl oysters would have revealed clearer responses

of the experimental groups to the effect of

nursery culture-late culture sequences on survival

(Monteforte et al. 1996). Further studies are neces-

sary to test for the effect of stocking densities and

cleaning schedules.

Acknowledgments

We dedicate this work to Don Gaston Vives, the

pioneer of pearl oyster culture in the world. Our

Pearl Oysters Research Programme is being funded

by the National Council of Science and Technology

(CONACYT, MeÂxico), the Research System of

the Cortes Sea (SIMAC, MeÂxico), the Mexican

Foundation for the Conservation of Nature

(FMCN, MeÂxico), the National Commission for the

Knowledgment and Management of the Biodiversity

(CONABIO, MeÂxico), and the International

Foundation for Science (IFS, Sweden). This is also

an institutional research project of the Centro de

Investigaciones BioloÂgicas del Noroeste, S.C.

(CIBNOR, La Paz, MeÂxico). Special thank to Mr

R. J. Roberts for his accurate advice and english

improvement on the manuscript. Our gratitude to

the colleagues of the Pearl Oysters Research Group

for all the SCUBA survey, data recording and

solidarity during all these years.

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