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Mucosal immunity in mollusks

Bassem Allam, Emmanuelle Pales Espinosa, in Mucosal Health in Aquaculture, 2015

12.14 The promise of new technologies

Recent progress in “omics” technologies provides the resources and tools needed to make significant
progress in our understanding of the role of mucosal immunity in mollusks. There are currently six more
or less complete molluscan genomes that are publically available: the pearl oyster Pinctada fucata, the
Pacific oyster C. gigas, the Mediterranean mussel (M. galloprovincialis), the owl limpet Lottia gigantea,
the California sea hare Aplysia californica, and the snail Biomphalaria glabrata. As well-assessed by Loker
(Loker, 2010), a synthetic comparative interpretation of the molluscan immunome is currently lacking
and should be addressed. Nevertheless, combined with new development in transcriptomic and
proteomic tools, this resource opens the door to thorough, in-depth investigations of the nature and the
dynamics of the effectors of mucosal immunity. Recent quantitative proteomic analysis (using a
combination of publically available genomic and transcriptomic resources as a reference) unraveled the
extensive diversity of defense-related molecules in oyster and mussel pallial mucus (Pales Espinosa et al.,
2014b). In oyster mucus, a total of 1,500 proteins were identified with about 200 matching proteins
known to be involved in immunity and defense against pathogens, including antimicrobial peptides,
lysozyme, several lectins, and other pathogen recognition receptors as well as several proteases and
protease inhibitors. While promising, these findings showing the diversity of antimicrobial molecules in
mucus are a clear reminder of the daunting little extent of our current knowledge on mucosal immune
effectors and their regulation in mollusks. More interestingly, mucus contained several proteins with no
match in current databases, highlighting the potential for the discovery of novel bioactive compounds in
these matrices.

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Immune responses in molluscs and their implications for disease control

B. Novoa, A. Figueras, in Infectious Disease in Aquaculture, 2012

3.2.9 Other immune molecules

Recently, several genes related to the inflammatory response against LPS stimulation have been detected
in bivalves. This is the case for the LPS-induced TNF-α factor (LITAF), which is a novel transcription factor
that critically regulates the expression of TNF-α and various inflammatory cytokines in response to LPS
stimulation. It has been described in pearl oyster Pinctada fucata (D. Zhang et al., 2009), C. gigas (Park et
al., 2008) and scallop C. farreri, where it is up-regulated in LPS-challenged, but not peptidoglycan (PGN)-
challenged, haemocytes (Yu et al., 2007).

Other TNF-related genes have been identified in the Zhikong scallop, such as a TNFR homologue (Li et al.,
2009) and a tumor necrosis factor receptor-associated factor 6 (TRAF6), which is a key signalling adaptor
molecule common to the TNFR superfamily and to the IL-1R/TLR family, which is involved in PGN
signalling (Qiu et al., 2009).

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Taxonomy and Phylogeny

Katsuhiko T. Wada, Ilya Tëmkin, in The Pearl Oyster, 2008

2.3.1.13 Remarks

The taxonomic status of the Akoya pearl oyster remains unsettled because of substantial morphological
variation within and among populations, local geographical isolation of some populations, transport by
humans, hybridization, and erratic taxonomic practice. Traditionally, three distinct species were
recognized to correspond to three biogeographic realms: Pinctada imbricata Röding, 1798 in the western
Atlantic region, Pinctada radiata (Leach, 1814) in the eastern Indian Ocean and the Red Sea regions, and
Pinctada fucata (Gould, 1850) in the Indo-Pacific region. The Japanese populations have frequently been
recognized to be distinct either at a species level as Pinctada martensii (Dunker, 1872) (Hayami, 2000) or
subspecies Pinctada fucata martensii (Kuroda et al., 1972; Habe, 1977, 1981; Matsukuma, 2004). The
distinctions were based either on continuous characters or on polymorphic and ontogenetic variations,
despite the fact that most authors expressed doubts of the utility of these characters.

Recent genetic analyses (Colgan and Ponder, 2002; Masaoka and Kobayashi, 2002, 2003, 2005a, 2006b;
Atsumi et al., 2004; Yu et al., 2006) based on a variety of genetic (allozymes, partial nuclear 18S and 28S
rDNA, internal transcribed spacers ITS1 and ITS2, partial mitochondrial 16S rDNA) have shown that the
populations from Australia, South East Asia, and Japan form a highly supported monophyletic group and
are most likely conspecific (Fig. 2.5). Moreover, morphometric studies did not provide means for
separating the three populations (Colgan and Ponder, 2002). In addition, mating experiments have
corroborated conspecificity of the South East Asian and Japanese populations (Atsumi et al., 2004).

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Figure 2.5. Neighbor-jointing tree of Pinctada species constructed with pairwise distances calculated
following the application of Kimura’s two parameter correlation for multiple substitutions in 28S rRNA
gene region. The tree was produced using MEGA 2. The numbers above the branches are the percentage
of 1000 bootstrap replicates. From Masaoka and Kobayashi (2005d).

Regarding the Persian Gulf populations, Beaurnent and Khamdan (1994) in their electrophoretic and
morphometric study of pearl oyster specimens from the Natural History Museum, London, indicated that
the Japanese shells clearly fall within the range of specimens from the Arabian Gulf. Masaoka and
Kobayashi (2006a), however, discriminated the Persian Gulf specimens from the Japanese specimens in a
phylogenetic analysis based on the hypervariable intergenic spacer of nuclear ribosomal RNA and
mitochondrial 16S ribosomal RNA gene regions.

Molecular studies showed that the Atlantic populations are differentiated from the Indo-Pacific
populations by phylogenetic analysis of partial hypervariable intergenic spacer of nuclear ribosomal RNA
genes (IGS) and the mitochondrial 16S rRNA gene regions, the loci commonly used for intraspecific
(population-level) analyses (Masaoka and Kobayashi, 2003, 2004a, b, 2005a–d) (Fig. 2.5).

Comparative karyotype analysis did not reveal any difference between the Atlantic (Caribbean) and the
Pacific (Japanese) populations (Wada, 1978; Komaru and Wada, 1985; Wada and Komaru, 1985). To date,
no discrete morphological characters were reported to be diagnostic of populations from the three
biogeographical regions.
Taken together, these studies suggest that the Akoya pearl oyster is a cosmopolitan, globally distributed
species, characterized by substantial intraspecific variation largely due to clinal genetic differentiation
and morphological plasticity. Considering disjunct distribution of some populations, incomplete sampling
of morphological and genetic data, and the lack of sound taxonomic revision, more research is required
to establish whether Pinctada imbricata, P. radiata, P. fucata and P. martensii comprise a single species
[as anticipated by Shirai (1994) although without providing justification for his claim]. Given the
paramount importance of members of this species complex in pearl culture, proper understanding of
phylogenetic affinities among different populations of this species complex has important implications
for the genetic programs in the pearl industry (Wada, 1982, 1984, 1994, 1997, 1999; Wada et al., 1995).

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Scallops

Maureen K. Krause, Elisabeth von Brand, in Developments in Aquaculture and Fisheries Science, 2016

Nuclear Genomes

Knowledge of the complete genome of any organism is a remarkably powerful tool to understand its
biology. The field of genomics encompasses more than just characterising the entire nucleotide
sequence of each chromosome for a species. Genomics generally refers to studies that use a multitude
of new high-throughput methods to study DNA, RNA, and organelle genomes for comparative,
functional, and environmental studies. Genomic approaches require the use of bioinformatics, highly
sophisticated computerised analyses that help decipher patterns and processes from the immense
volume of data generated. Twenty-first century bivalve genetics will probably best be characterised by
the giant leap forward from studies of one to few genes to new genomic approaches. For bivalve
molluscs including scallops, there is tremendous potential to apply information from genomics to
immunology, aquaculture, fisheries, and evolution that are just beginning to be realised.

At the time of publication of the last edition of this book, Beaumont was able to compile a detailed table
of the karyotypes of several scallop species and mentioned a few early attempts at genetic mapping
using newer molecular markers (Beaumont, 2006). Since then, knowledge of scallop genomes and
chromosome structure has advanced considerably. For bivalve molluscs, draft genomes are publicly
available only for the oyster Crassostrea gigas (Zhang et al., 2012a) and for the pearl oyster Pinctada
fucata (Takeuchi et al., 2012). It was just announced that two complete scallop genomes will be
published in 2015 (Wang, personal communication) According to Shi Wang, the Ocean University of
China recently completed genome assemblies for Azumapecten farreri (NCBI Bioproject ID 185465) and
Mizuhopecten yessoensis (NCBI Bioproject ID 253231). They are in the process of publishing their work,
but presented their preliminary findings at World Aquaculture 2014 meeting. For M. yessoensis, the final
genome assembly is 999 Mb, and predictions estimate that it contains approximately 23,000 genes. They
found that tandem repeats and transposable elements dominate the genome, accounting for 44% of the
genome. Evidence for active transposition is supported by independent sequence data from Yoshida et
al. (2011), showing that the largest gene family in M. yessoesis is an endonuclease-reverse transcriptase
(Genbank accession number FC614452) present in approximately 1200 copies in the total genome.

Once publicly available, it is anticipated that the genomic resources will be enormously useful for
understanding scallop biology and the molecular genetics mechanisms responsible for controlling
production-related traits. Another important genetic resource for scallops will be the availability of
complete genome-wide physical maps of the chromosomes. These maps estimate the true distance, in
nucleotide pairs, between regions of interest. When they are linked to genetically mapped markers they
can be powerful tools to improve genome assembly, identify loci associated with phenotypic characters
of economic and scientific interest and integrate genome information. These maps are typically
constructed by detecting regions of overlap and then ordering large, cloned fragments of DNA including
those in bacterial artificial chromosomes (BACs) and fosmid (Meyers et al., 2004) vectors. BAC (Y. Zhang
et al., 2008b) and fosmid (Cheng et al., 2008) libraries exist for A. farreri, and the BAC library was
successfully used to identify genes related to immune function (Zhang et al., 2008c; Zhao et al., 2012).
The first complete physical chromosome map for a mollusc was produced for A. farreri in 2011 (Zhang et
al., 2011).

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Research Methods in Biomineralization Science

Christopher E. Killian, Fred H. Wilt, in Methods in Enzymology, 2013

3.2 siRNA loss of function in the mollusk shell

RNA interference (RNAi) is a relatively recently discovered regulatory pathway that uses double-stranded
RNA molecules to selectively destroy specific mRNA molecules. It is part of the normal armamentarium
of many plants and animals. Small double-stranded RNA (dsRNA) molecules can be generated from long
precursor dsRNA by an endonuclease named Dicer, which cleaves the long dsRNA into short double-
stranded fragments—usually about 20 nucleotides long. The short dsRNA is named siRNA (small
interfering RNA). The siRNA is unwound into two single-stranded RNAs, one dubbed the “passenger,”
whereas the other named “guide.” The passenger strand is degraded, and the guide strand is
incorporated into a multicomponent silencing complex (called RISC). In instances where the guide strand,
incorporated into a RISC complex, can anneal by base pairing with a complementary sequence in an
mRNA, a nuclease, named Argonaute, embedded in the RISC will cleave the mRNA, thus rendering it
inactive. The decreased expression of the gene and its mRNA is thereby accomplished.

The strategy employed in the mollusk shell construction, and in many other instances, takes advantage
of this normal cellular mechanism for regulating gene expression. The crucial step is to synthesize, in
vitro, a long dsRNA corresponding to the presumptive mRNA of a gene suspected to have a role in
biomineralization. Suzuki et al. (2009) used this approach. These researchers identified an acidic protein
named Pif from the nacre of the shell of the pearl oyster, Pinctada fucata, which binds to aragonite. They
employed the RNAi strategy to demonstrate that Pif did, indeed, play a crucial role in nacre construction.
In conjunction with immunolocalization of Pif and studies of aragonite formation, in vitro, they built a
strong case for the role of Pif in biomineralization. There are several steps required to carry out this type
of experiment; we can illustrate this by looking at the experimental protocols used by Suzuki et al.

3.2.1 Identify a protein of interest, and determine its amino acid sequence

If possible, determine the nucleotide sequence of the mRNA used for synthesis of the protein. The nacre
from the pearl oyster was decalcified with acetic acid, and the insoluble matrix was dissolved in the
detergent, sodium dodecyl sulfate, and a reducing agent (dithiothreitol), incubated with either calcite or
aragonite. The minerals were then washed with small amounts of water, and the eluants examined by
acrylamide gel electrophoresis. Almost all the proteins were eluted with water, but in the case of
aragonite, one band on the gel, comigrating near 80 kDa, was missing. This putative aragonite-binding
protein did not bind well to calcite and was used for subsequent investigation.

3.2.2 Synthesize, in vitro, a long dsRNA molecule corresponding to the mRNA of interest

The next steps used are conventional molecular biology. The 80 kD band was excised from the gel, the
protein eluted, and some amino acid sequence obtained by sequencing fragments of the protein. These
amino acid sequences are then used to design PCR primers (Apte & Daniel, 2009; Telenius, Carter, Bebb,
Ponder, & Tunnacliffe, 1992). Since, in this case, the gene had not been cloned and the exact nucleotide
sequence encoding it was not known, it was necessary to use degenerate primers, that is, all four bases
are employed for the different codons of each amino acid. PCR was employed to isolate a cDNA from
RNA extracted from the mantle. By careful control of annealing conditions during PCR cycles and by
sequential use of nested primers, a cDNA representing the Pif protein was obtained from the mantle
mRNA. A full-length cDNA was obtained by the RACE PCR strategy (Frohman, 1990).
The cDNA sequence was determined, and primers were designed to produce a long dsRNA
corresponding to this mRNA. Both primers included a sequence corresponding to the promoter for T7
RNA polymerase, so that the cDNA produced by PCR could then be used for synthesis of both strands of
a dsRNA, in vitro. The two RNA strands thus produced were annealed to one another and used in the
subsequent experiments. Similar steps were used to produce a control dsRNA, one that would not be
expected to produce a knockdown of biomineralization. These workers used an mRNA for GFP (green
fluorescent protein) as a control.

3.2.3 Introduce the dsRNA to the biological system being examined

Getting a highly charged, high-molecular-weight polyelectrolyte into cells can be challenging. There are
many choices, and one advantage of the exogenous RNAi is that, in some organisms, the process is
known to spread in an intact organism from one organ system to another. In the case of the mollusk
nacre, the investigators injected different amounts (volume was kept constant; amounts ranged from 5
to 30 micrograms) into the adductor muscle and then waited 7 days to carefully inspect the nacre.

3.2.4 Monitor the effect of the introduced siRNA

It is crucially important to monitor, hopefully by several means, whether the RNAi has actually lowered
the concentration of the mRNA of interest. This is often done by quantitative PCR. Primers already used
in production of the dsRNA can be used. Suzuki et al. (2009) examined Pif mRNA levels in the RNA
extracted from mantle by qPCR and showed a concentration-dependent lowering of mRNA levels by
approximately 50%. Examination of the nacre made after RNAi treatment showed that it was disordered
and addition of new layers of nacre had been halted. Since control dsRNA had no such effects, they had
compiled a strong case for an important and necessary role for Pif in elaboration of nacre.

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Pearl Oyster Culture

Paul C. Southgate, in The Pearl Oyster, 2008

7.5 CULTURE INFRASTRUCTURE

Pearl oysters are sub-tidal animals that can generally tolerate only minor emersion. Culture apparatus
must account for this and pearl oysters are generally farmed using suspended-culture systems such as
rafts or longlines, or bottom culture systems such as fencelines, racks or tressles. Gervis and Sims (1992)
listed the following criteria as the basis for the choosing between these different culture systems:

current speed

water depth

capital cost

operational costs

exposure to wind and waves

ease of operation

need for direct access from land

•
security considerations

tidal variation.

7.5.1 Rafts

Rafts are rigid floating structures composed of a framework from which culture apparatus containing
pearl oysters can be hung (Fig. 7.9). They are commonly made from bamboo, timber or plastic pipe.
Buoyancy is provided by attached floatation devices such as barrels, plastic container, drums and floats.
Rafts commonly have 4–6 floats of 200–300 L capacity and, as a “rule of thumb”, each 200 L barrel can
support around 200 kg (Quayle and Newkirk, 1989). The material from which rafts are made generally
reflects what is locally available. Raft size varies but the traditional Japanese raft measures 6.4×5.5 m and
has four 0.6×1.05 m styrofoam floats (Gervis and Sims, 1992); it provides 100 points for attachment of
oyster culture units.

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FIGURE 7.9. Raft used for pearl culture in Li’an Bay, Hainan Island, China.

Rafts may be moored to fixed structures such as jetties or anchored independently to maintain position.
The former provides convenient access to culture stock and negates the need for a boat. Rafts are more
commonly deployed in sheltered areas with relatively low wind and wave action where a number of rafts
may be moored together. The relatively low-cost and simple construction of rafts are advantageous, and
the work platform that they provide (Fig. 7.10) allows culture stock to be inspected and accessed without
the use of divers. Perhaps the major disadvantage of rafts is the relatively close proximity of culture units
holding pearls oysters which has implications relating to water flow and water quality, food availability
and the spread of disease (Gervis and Sims, 1992).

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FIGURE 7.10. Rafts in Li’an Bay, Hainan Island, China, provide a work platform for care and maintenance
of pearl oysters (e.g. cleaning and grading) and cleaning, repair and storage of culture equipment.

7.5.2 Longlines

Longlines are composed of a large-gauge rope, or headline, supported by floats, that is anchored at
either end to maintain position (Fig. 7.11). The headline provides an attachment point for “dropper”
ropes to which culture apparatus containing pearl oysters are attached. Longlines are better suited to
wind and wave exposure than rafts and their smoother movement under such conditions results in less
wear and tear on the anchoring system and reduced impact on oyster growth. Longlines may be
constructed to float on the ocean’s surface (“surface longline”) or may be deployed in mid-water (“sub-
surface longline”).

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FIGURE 7.11. Longline used for Pinctada maxima culture in northern Australia. Note the panel nets
containing pearl oyster juveniles suspended from the longline. (Photo: Clare Flanagan.)

Surface longlines are extensively used for the culture of Pinctada fucata and Pteria penguin in Japan and
for Pinctada maxima in Australia and Indonesia (Figs. 7.11 and 14.3). In Australia, surface longlines are
generally 100 m long and deployed parallel to each other at 20–30 m intervals to avoid entanglement
with adjacent lines (Wells and Jernakoff, 2006). Floats are placed at 1–2 m intervals and dropper ropes
supporting culture apparatus (see Section 7.5.4) are attached at 1 m intervals (Fig. 7.11).

Both rafts and surface longlines provide a floating substrate from which culture units containing pearl
oysters can be attached. However, potential problems associated with their use include surface
movement that may affect the growth rate of pearl oysters, potential navigational hazard and potential
security issues because of their visibility. Sub-surface longlines are less prone to these problems;
however, they are more difficult to deploy and rely on scuba divers for regular maintenance and
inspection. Sub-surface longlines are widely used in French Polynesia and the Cook Islands for culture of
P. margaritifera.

7.5.3 Racks, tressles and fencelines

Racks or tressles are composed of a rigid framework fixed above the seabed using legs or other supports.
They can be made from timber poles, or metal or plastic pipes to provide a platform onto which culture
units containing pearl oysters can be placed or hung. Tressles are relatively low cost and simple to
construct, require low maintenance and, being on the bottom, are less prone to adverse weather
conditions and security risks. However, they are only assessable using SCUBA and cleaning is more
difficult and labor intensive than with surface culture apparatus. Tressles have been used for pearl oyster
culture in Australia, Sudan and Mexico and are the traditional culture system for culture of Pinctada
margaritifera in French Polynesia and the Cook Islands (Coeroli et al., 1984). In response to disease and
oyster mortality resulting from overcrowding and poor water quality, tressles have been replaced by sub-
surface longlines in Polynesia (Gervis and Sims, 1992) resulting in reduced oyster densities and improved
water circulation (Sims, 1993a).

Fencelines utilize strong galvanized metal posts driven into the substrate, as supports for a line which is
raised above the seabed. Culture units containing pearl oysters are hung from the line. Fencelines are
generally used in relatively exposed sites in Western Australia (Wells and Jernakoff, 2006) and, while the
capital cost of a fenceline is less than that of a surface longline, like tressles, they are more difficult to
deploy and rely on divers for regular maintenance and inspection.

7.5.4 Culture units and methods

Various culture apparatus are used for ocean-based culture of pearl oysters. Most commonly used are
pearl nets, panel nets, lantern nets and box nets. Nets are generally constructed from galvanized or,
more commonly, plastic or powder-coated metal frames covered with polyethylene netting of varying
mesh size appropriate for the size of cultured oysters. Pearl nets (Fig. 7.12) and lantern nets are
commonly used to hold juvenile pearl oysters in large numbers, prior to their deployment to larger
culture units (Gaytan-Mondragon et al., 1993). Very often, they are used to hold oysters following their
removal from spat collectors at grading. Panel nets, also known as pocket nets (Fig. 7.13), are composed
of a strong frame covered with mesh that is sewn to form pockets to hold oysters. The size of the pocket
and the size of the mesh can be altered, depending on species and the size of the cultured oysters. For
example, panel nets used for small juveniles may have 48 pockets and be composed of 5 mm mesh,
while those used for adult Pinctada maxima are likely to have six pockets made from 30–45 mm mesh.
Clearly, the mesh size needs to be as large as possible to maximize water flow and food supply and
minimize fouling.

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FIGURE 7.12. Pearl nets used for culture of Pinctada margaritifera juveniles in the Cook Islands. (Photo:
John Lucas.)

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FIGURE 7.13. Panel nets containing Pinctada maxima being inspected by a diver at a pearl farm in north
Bali, Indonesia. (Photo: Joseph Taylor, Atlas Pearls.)

Perforated plastic trays and baskets are also used for holding pearl oyster spat and juveniles. Plastic trays
(55×30×10 cm) with lids have been used to hold spat collectors containing P. margaritifera following
transfer from the hatchery until grading (Southgate and Beer, 1997) and have been used during nursery
culture of P. margaritifera (Friedman and Southgate, 1999a; Southgate and Beer, 2000; Whitford, 2002).

7.5.4.1 Ear-hanging

Pearl oysters are commonly cultured using the “ear-hanging” method in Polynesia (Fig. 7.14). It involves
drilling a small hole (∼2–3 mm) through the base of the shell in the dorsal-posterior region.
Monofilament fishing line or wire can then be used to attach oysters to a rope that is itself attached to
either a raft or longline. A number of oysters are usually attached to a single rope (Fig. 7.14) which is
generally referred to as a chaplet (Friedman and Southgate, 1999b). Oysters can be attached singly or in
pairs. The advantages of ear-hanging include greatly reduced outlay for culture equipment and, given
that the cultured animals are not enclosed within a culture unit, there is greater flow of water and
improved food availability. However, without any protective housing, they are prone to predation.

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FIGURE 7.14. Pinctada margaritifera attached to chaplets at a pearl farm in Takapoto Atoll, French
Polynesia. (Photo: John Lucas.)

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Introduction
Elisabeth Strack, in The Pearl Oyster, 2008

1.3.1 Persian Gulf

The first reference is found in an Assyrian inscription that dates back to around 2000 bc, speaking of “a
parcel of fisheyes from Dilmun”, probably pearls from Bahrain, where the Dilmun civilization was
centered from 3,200 to 1,600 bc. In 1989, a 4 mm pearl, estimated to be about 4,000 years old, was
found in a Dilmun settlement.

Probably the oldest known pearl necklace comes from an Achemenid grave at the Acropolis of the
Winter Palace of the Persian kings in Susa, dating back to the middle of the 4th century bc. The necklace
came in 1908 to the Persian Gallery at the Louvre in Paris. It was discovered during an expedition by
Jacques de Morgan in 1901. The regularly arranged pearls are sized between 3.5–7 mm, with baroque to
barrel shapes. Some pearls of a white to grayish color have been preserved well over the period of
nearly 2,500 years and reveal a near perfect luster.

Pearl grounds originally stretched on the Arabian side from Kuwait along the coast of Saudi Arabia to
Bahrain, Qatar, the United Arab Emirates and the Sultanate of Oman (Fig. 1.5). They also run along nearly
the whole coast of the Persian side of the Gulf, from near Bandar-e-Busehr (island of Khark) to Bandar-e-
Lengeh (island of Kish) in the south, and even further south into the Strait of Hormuz (Fig. 1.5).

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Figure 1.5. The Persian Gulf and Red Sea coasts.

The Phoenicians, who probably held the first monopoly of the pearl trade, were succeeded by Arab
seafarers, undertaking long and difficult journeys with their sailing ships of simple construction, the so-
called dhows. The city of Masqat (Muscat) in the Gulf of Oman was the main trade center. After 1515,
when Alfonso d’Albuquerque came to the Strait of Hormuz, the Portuguese brought the pearl fisheries
under their control. In 1622, the Persian Shah Abbas took victory over the Portuguese, and the new
harbor town Bandar-e-Abbas on the Persian side became the new center. The pearl fisheries returned to
the control of the local sheikhs who generously allowed their subjects to fish for pearls for a small fee.
Jean Baptiste Tavernier, who visited the city of Ormuz in 1670, described pearl trading in the Gulf in his
memoirs.
The last boom time was between about 1850 and 1930 and when it was over, partly due to the world
economic crisis of 1929 and partly due to the advent of the cultured pearl, pearl fishing went into a
decline. The countries at the Gulf were saved just in time from falling into poverty by the discovery of oil
in 1932.

There are Akoya pearl oysters1, known locally as “mohar”, in the Persian Gulf and most of the so-called
oriental pearls were obtained from these. In the past, the species was often described as Pinctada
vulgaris or the “common Pinctada” in gemmological literature. Akoya pearl oysters grow to shell length
60–80 mm in the Gulf, with a life-span of 7–8 years. They live on sand banks and coral rocks. The thin
shells show a white, cream or pale yellow MOP, and pale pink to somewhat violet is occasionally
observed. The MOP industry did not start using the shells until the 19th century. Until World War II, large
quantities were imported to London and Hamburg under the name “Lingah-Persian Gulf”. They were
mainly processed into cheap buttons used for uniforms and undergarments. The Japanese called the
shells “shinju” (pearls). Exports were mainly handled from Basra, which even before the 19th century
had been a center for the export of shells to other Arabian countries and India, where they were used for
intarsia and also in the production of pills and betels.

The “Lingah Shells” were named after Lingah, a small place on the Arabian side of the Gulf. The term was
soon used generally for small and thin shells, and traders started referring to “Ceylonese Lingah”,
“Australian Lingah” or “Venezuelan Lingah”, depending on the place of origin. Other names used for the
shells from the Gulf were “Bastard Shell” and “Lapi Shell”.

Pinctada margaritifera is also found in the Persian Gulf, hence the geographical name P. margaritifera
persica from Jameson (1901). The Arabian names are “sudaifee” or “zinni”. They may grow to 200 mm
shell length in the Gulf. The color of the MOP is cream to light gray. Indian dealers probably purchased
the shells since early times, as the 19th century MOP trade called them “Bombay Shell”. Over the
centuries, the shells have probably been of greater commercial significance than the pearls. In 1908,
during the high time of the MOP industry, ca. 3,000 of shells were exported. Around the middle of the
19th century, approximately 60,000 people, nearly the whole population of the Arabian side of the Gulf,
worked in the pearl fisheries. The fishing season was usually concentrated between April and September.
At first the shallow coastal waters were fished, leaving the deeper grounds for the warmer season. The
grounds were fished in rotation in order to ensure they were left fallow for several years. The pearling
fleets were centered in Bahrain and in Doha in Qatar (Fig. 1.5). They consisted of about 150 ships in the
tradition of the dhows that were usually owned by rich merchants, often from India, the so-called
“bunnias”. An important person aboard the ships was the so-called “nahhams” who sang the ritual
prayers that determined the schedule of the day. The captain, called “nokhata”, had absolute command
of the divers, the so-called “ghai ghawwas” who lived and worked on the ships. The divers used
characteristic utensils like a wooden nose clamp (fitaam), cotton tampoons trenched in oil for the ears, a
basket (dadjin) to hold the molluscs and a knife for cutting them off from the bottom. On their fingers
and toes they wore small leather caps, the “khabbal”. A diver descended on two ropes that his assistant,
the “saib”, held and controlled from the ship (Fig. 1.6). He remained underwater for 60–90 seconds,
reaching a depth of 6–20 m. Each diver would usually descend 30 to 40 times in one day and there were
usually 8 to 40 divers on one ship. A crew of 20 to 30 divers could harvest 7,000 to 8,000 pearl oysters
per day. The whole pearling fleet harvested a total of approximately 150 million pearl oysters during
certain seasons. Modern diving suits, coming into fashion around 1900, were not used initially and were
later prohibited by the sheikhs in order to further avoid overfishing.

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Figure 1.6. Pearl at work in the Persian Gulf. (Photo: Falcon Cinefoto Bahrain.)

The pearl oysters were opened on deck with a knife; large pearls were removed immediately by hand
and the rest were harvested using 25 brass sieves, the so-called “tasah”. As a rule there were several
small pearls in each 500 pearl oysters. Pistol shots heralded the lucky find of a large pearl, the sound of
which could be heard in far away places on the coast. All pearls were eventually collected by the captain
in the traditional red cloth and after he had sold the first pearls he paid the divers in cash. They received
the lowest part as they were on the lowest end of the hierarchy and were usually caught in a vicious
circle of poverty from which they could not free themselves.

The pearls were usually purchased by middlemen, the so-called “tawwash”, who came directly to the
ships and sold the pearls on to larger dealers. The pearls dominated life in the Gulf for centuries and they
once dominated the world trade as “oriental pearls”. Currently, pearls from the Gulf are sold to Indian
pearl dealers who clean, bleach and drill them in India, from where they are sold internationally and are
also sold back the Gulf states.

New pearls from present fisheries account for only 15% of the trade and are still called “Basra pearls”. All
pearls entering Bahrain are examined by the Gemstone and Pearl Testing Laboratory, which was
established by the Ministry of Commerce in 1990.
About 4,000 to 5,000 pearls of good quality were fished each season during the boom years between
1850 and 1930. Colors range from white to dark cream and very light pink. There are even yellowish-pink
pearls that resemble the apricot hue of today’s Chinese freshwater cultured pearls. Arabian language
calls them “nabatee”, the word for sugar of the same color. Nevertheless white pearls achieve the
highest prices. The majority of pearls are small and irregular in shape, mainly 4–6 mm in size. Pearls of
8–9 mm in size are exceptions, and supposedly originate from P. margaritifera. Round or nearly round
shapes are rare, usually the pearls are slightly to distinctly off-round or slightly baroque.

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