1. Introduction
Humans have long exploited bivalves as sources of food and products used in materials/building, concrete, fertilizer, and cultured pearls. Indirect benefits include shoreline stabilization and nutrient mitigation
[5][1]. Other indirect benefits accrue from the fact they are filter feeders, and accumulate microorganisms and heavy metals
[11,12][2][3]. These properties may mitigate pollution, but render the meat dangerous; however, they mean that bivalves such as the windowpane oyster
P. placenta can be useful proxies for monitoring the quality of coastal waters. More recently, molluscs have been studied as a source of novel bio-active molecules.
2. Historical Perspective of Exploitation
Windowpane oyster is the name given by travellers in Southern China, which is derived from the use of the shell.
P. placenta shells were extensively used in the Portuguese settlements in 1675 in India, because of the scarcity and cost of window glass. At the start of the 20th century, window glazing was seen in the Dutch Indies, in the Philippines, and in Canton and other districts of Southern China. The Chinese were the first to utilize the shell, and dissemination of this use is credited to the Portuguese
[6][4], though without further historical evidence, this may reflect a European colonial perspective, since the extensive trading empires in Asia, e.g., the Austronesian
[13][5] and later Indian maritime traders
[14][6], may well have spread this practice.
P. placenta meat is edible, though the oyster has unusually extensive mucus, well above the small amount used to produce pseudo faeces in other molluscs. This mucus is simply removed by washing when preparing the meat (
Section 4.1.2). While pearls of inferior quality are yielded in some quantity, it is the translucent shell that is today commercially and economically important. However, this was not always the case.
Placuna placenta provided a fishing industry of local importance in four widely separated localities in eastern seas. Shells for glazing were half-grown (about 18 months old). These were then cleaned and polished by soaking, tossing, and shaking several times until dirt and roughness were removed and a translucent mica-like appearance was obtained
[6][4]. Interestingly, there was a seed pearl fishery in North Bornean waters, which was less well-known, and therefore able to provide for sustainable exploitation by the Badjao divers (Malay inhabitants who, at the present time, are one of the cultural minorities in the Philippines currently known as sea gypsies, and scattered along the coastal areas of Mindanao)
[15][7]. Historically, in this community, no shell was allowed to be fished under 10 cm in diameter and a license granted by the village chief (the duration of its validity is not recorded) was required before shells could be harvested. Badjao women and children shucked the shells, and pearls were obtained by slowly heating the meat over 3 days. After thorough cleaning, seed pearls obtained by the Badjaos were sold to Chinese dealers and exported to China where the bulk was used in preparation of folk medicines for the treatment of eye diseases and syphilis. Similarly, small pearls from Ceylon were also brought to India for use as components in native medicines or as a cosmetic, while bigger pearls were sold separately.
Placuna placenta pearls have low value because of their small size, poor luster, irregular shape, and lack of hardness compared to gem pearls and the fanciful beliefs and traditions regarding medical uses of the pearls diminished with the progression of evidence-based medicine. However, the implementation of rules to govern
P. placenta harvesting provides inspiration for the present day.
Philippine history traces the popularity of the shells to the 1860 edition of “Vocabolario de la lengua Tagala”, the first dictionary of the Tagalog language
[16][8]. Within it, the entry for capiz reads la Ventana (window). Pre-colonially, seashells were widely used in building, weapons, decorating clothing, and trading goods
[17][9]. During Spanish colonization, churches and homes were built using capiz shells as a substitute for glass. Thus,
P. placenta was the most common type of window material used in the Philippines between 1755 and 1960. The thin translucent shells were individually squared and then set like glass panes into wooden lattice frames to be used as window shutters, a unique feature of Philippine architecture from the Spanish colonial period (
Figure 1). This includes the sliding windows of the 19th century. Such windows are also found in Goa in India. Today, the shells, are used in the manufacture of decorative items such as chandeliers, Christmas decorations, windowpanes, and many more
[18][10], and from 1960, the shell served as the raw material of a lucrative export-oriented shell craft industry (
Figure 2). Thus,
P. placenta shell products are among the Philippines’ most important fishery exports.
Figure 1.
Example of a traditional Capiz window (photograph JMR, 20 June 2023, Samal, Bataan, Region III, Philippines).
Figure 2. Examples of commercial products made from Capiz shells (Photograph JMR, 10 July 2023; Kaliwanag Rural Improvement Club; San Juan, Samal, Bataan, Region III, Philippines).
3. Modern Economic Exploitation
P. placenta was once very abundant along the Philippine coastline. Before World War II,
P. placenta processing was a lucrative industry in the province of Bataan. It is one of the indigenous seashells originally found in Samal and in the nearby municipalities of Abucay, Balanga, Pilar, Orion, and as far as Limay. However, the population of these bivalves has decreased. Contributing factors include the mechanized boats used by fishermen in collecting small pieces of stones or chips of sea shells locally known as “gasang”, which destroys the natural habitat of the bivalve, and destructive methods of fishing and gathering such as trawling, using mechanical rakes and dredges, dynamite fishing, and compressor diving
[10][11]. Thus, the high demand for this bivalve, both locally and internationally, has resulted in over-harvesting and habitat degradation
[17][9]. In addition, the increase in prawn hatcheries may have also contributed to the decline in
P. placenta harvests. In the late 1980s, prawn hatcheries flushed water laced with antibiotics back to the sea and the contamination may have killed
P. placenta [19][12]. The result is a documented decline in harvest and revenue, recorded both locally and nationally.
Locally, in Bataan, based on the records of the Bataan provincial Agriculturist’s Office in 2016, 248 tonnes of
P. placenta were harvested and there was a reduction in the harvest of the shellfish to 154 tonnes in 2017 and to 138 tonnes in 2018; a 45% decline in just two years. The same scenario was repeated across all regions of the Philippines where
P. placenta are harvested. Thus, the national export of shells and by-products for the country as a whole showed a substantial decline from 3260 tonnes in 1994 to 1765 tonnes in 1999, and just 731 tonnes in 2021
[2,20,21,22][13][14][15][16]. Consequently, the export of
P. placenta products, which had an important economic impact on the Philippines, has suffered a major decline. From ranking fifth among the major fishery exports in 1991, and generating USD 33.5 million from 1989 to 1991 in shell crafts
[23,23][17][17], it declined (USD 7.15 million in 1994
[22][16], USD 4.45 million in 1996
[21][15]) to USD 1.085 million in 2021
[2][13].
A combination of legal and remedial measures have been taken to try to reverse the decline of the
P. placenta fishery. The Department of Agriculture Bureau of Fisheries and Aquatic Resources is responsible for implementing fishery regulations. Marine Protected Areas (MPAs; “no-take zones”) have been established and these and other marine areas are protected by law from destructive activities. However, there is little that is directly applicable to
P. placenta and much activity is devolved, for practice and implementation, by concerned institutions and fisheries agencies according to their programme mandates. There are monitoring systems and co-management by local communities/stakeholders, but there is no robust data acquisition to provide evidence relating to compliance or enforcement, which in part explains the continued decline of
P. placenta harvests
[24][18].
Some remedial measures have been taken, though these have been local, rather than across the entire historical range of
P. placenta. Researchers of the Bureau of Fisheries and Aquatic Resources of the province of Bataan, Philippines, demonstrated that stock enhancement of
P. placenta breeders can be made possible by enclosing a certain area using bamboo fencing with nylon nets, and by letting the oyster breed naturally. They recommended that the strict implementation of fishery laws, rules, and regulations could increase the production of the bivalve in the province
[25][19]. In another study, it was found that the transplantation of
Placuna placenta was feasible. Survival after three months of the oysters transplanted during the rainy season was 35–48% and 57–60% for those transplanted in the dry season, though larger ones only grew during the dry season. Gonad sizes also increased in weight over the three months, but more during the dry season. Among the larger individuals, gonads matured 3–4 months after transplantation and 60% of the animals spawned in June
[26][20].
Placuna placenta with an average shell length of 10 cm were successfully spawned by raising the water temperature to 29 ± 0.5 °C. Three water treatment schemes were tested for larval rearing: chlorination, ultraviolet irradiation, and filtration (control). Larvae survived to the umbo veliger stage (180 μm, day 10) in chlorinated seawater, whereas mass mortality occurred at the straight-hinge stage in both UV-treated and filtered seawater. Eggs measured 45 μm on average, and fecundity was 5000–10,000 per female. Larvae were reared on a combination of the microalgae
Isochrysis galbana, Tetraselmis sp., and
Chaetoceros calcitrans, maintained at a density of 100,000 cells/mL
[26][20]. It appeared that the combination of the diatom
I. galbana and the green alga
T. tetrahele enhanced gonad development in
P. placenta more than using single algal species
[27][21]. The Tigbauan coast, Iloilo, Philippines, had been depleted of the natural population of
P. placenta, but retained the conditions necessary for their growth and development. Benthic organisms associated with plankton species needed by the animals for food were still abundant and, therefore, oysters could naturally repopulate the area. To achieve this, stocking was carried out during the first and last quarters of the year to avoid the rainy season, which could affect the restocking
[10,28][11][22].
There are limited data on the efficacy of restocking, notably in the Panay Gulf beds. In 1999, it was confirmed
P. placenta juveniles were observed within a year of restocking. However, gatherers collected the juveniles, including by means of illegal methods (trawls, dredges) despite calls to allow juveniles to mature and breed several more generations and the deployment of markers and buoys
[29][23]. Thus, while there are fisheries regulations to control harvesting to protect the oysters and initiatives to restock, the high market demand for the shells and a lack of education, enforcement, and compliance results in gatherers continuing to collect shells with sizes less than 80 mm and more than 100 mm, and natural resources continue to be depleted
[19][12].
4. Nutritional Benefits of Bivalves
Fish and seafood such as molluscs play a key role in human nutrition. Edible molluscs such as mussels, clams, scallops, and oysters are naturally low in carbohydrates, e.g., raw scallops, oysters, and mussels have been reported to contain between 3% and 5% carbohydrate
[30][24], and lipids, but have a relatively higher content of unsaturated fatty acids. Moreover, they can be excellent sources of omega-3 fatty acids, vitamin B12, choline, and minerals such as iron, selenium, and zinc, and, in this context, have a similar or better nutrient value than some shellfish and land-based protein sources
[30,31][24][25]. Marine bivalves are considered nutritious because they have high-quality protein, containing all the essential amino acids
[32,33][26][27], as summarized by the proximate analysis of a number of bivalves.
Calcium is an essential component of the calcium carbonate shells of molluscan shellfish and it is recruited from seawater and deposited at fairly high concentrations in their tissues
[30][24]. Thus, levels of calcium in shellfish are 2- to 10-fold higher than those found in beef, chicken, or pork. The United States Department of Agriculture National Nutrient Database shows that raw oysters and mussels are an excellent source of iron, with clams and scallops containing less iron. Thus, while scallops contain less than half the levels of iron of beef, chicken, and pork, oysters, mussels, and clams contain several times the amount of land-based meats
[30][24]. The high levels of minerals found in molluscs are also reflected in
Placuna placenta. Because of the high iron content, a three-ounce serving of
P. placenta provides 44% of the daily recommended intake. Although iron is important for red blood cell count, this mineral may cause hemochromatosis or the over-absorption of iron in the digestive tract
[30][24]. However, a significant proportion of the population is moderately to highly iron deficient, and in the Philippines, zinc deficient too, the former being most common in women of reproductive age
[37][28]. A number of essential vitamins are also present. Of particular note is vitamin A, as deficiency in this vitamin can cause blindness, a problem that is prevalent in rice-based diets such as that found in the Philippines
[38][29]. This highlights the potential of
P. placenta to address this issue, at least in part.
Bivalve lipids have appreciable proportions of omega-3 long-chain polyunsaturated fatty acids (PUFAs), particularly eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). Generally, the contents of PUFA are higher than those of saturated fatty acids and monounsaturated fatty acids (MUFAs)
[41][30]. The contents of EPA and DHA in shellfish usually range between 300 and 500 mg% in raw muscle, and are generally lower than those of oily finfish such as Atlantic mackerel, salmon, and sardines
[33,42][27][31].
5. Pathogens, Allergens, and Contaminants in Bivalves
It is common to consume marine bivalves raw, steamed, or lightly processed
[44][32]; consequently, they can act as vectors of a variety of pathogens. This issue is compounded by the fact that bivalves are filter feeders and pathogen pollution is increasingly common in coastal waters. Moreover, bivalves contain allergens that can have major effects on susceptible people. Finally, the high content of certain nutrients can cause health issues.
The presence of microbial pathogens and parasites because of the pollution of coastal waters can result in the contamination of bivalve shellfish by a variety of microorganisms
[33,47][27][33], a problem compounded by the fact that bivalves are filter feeders and so can accumulate these pathogens in their tissues or organs
[46][34]. The resistance of some of these pathogenic microorganisms to antibiotics and the tolerance of bivalves to heavy metals such as copper, lead, and cadmium can add further risk. The habit of consuming raw or lightly cooked bivalves increases pathogen-associated risks. Food-associated parasites are recognized as a threat to food safety and human health. Increasing globalization of the food supply, the trend of consuming food raw, and general ignorance about parasites add to this hazard
[33][27].
The main helminth parasites of bivalves are trematodes, cestodes, and nematodes. Trematodes larvae are more important as bivalve pathogens than cestodes and nematodes. Infection in bivalves is most common in tropical and subtropical waters, where elasmobranchs constitute an important proportion of the vertebrate fauna
[45][35].
Giardia,
Cryptosporidium, and
Toxoplasma, which are major parasites of humans and animals, may retain their infectivity in raw or undercooked molluscs. These are transmitted by contaminated water and food and can cause human gastroenteritis.
Some parasites are not pathogenic to humans, but may reduce the visual appeal of oysters, such as pea crabs. However, no serious parasites have been detected in stocks of commercially edible P. placenta in the Philippines.
In addition to the possibility of hemochromatosis alluded to above, oysters may cause stomach problems because of their zinc content; 85 g of oysters can contain 67 mg of zinc, which is enough to trigger gastrointestinal reactions, because it is more than the tolerable upper intake level of 40 mg per day. These reactions include vomiting, diarrhoea, and abdominal cramps. The problems caused by the zinc in oysters generally arise within 3 to 10 h of consumption and quickly fade after zinc levels return to normal
[30][24].
Molluscan shellfish are also recognized as important food allergens. The prevalence of molluscan shellfish allergy is largely unknown, but may have parallel consumption patterns, with higher frequency in areas of frequent consumption
[49][36]. The major allergen of molluscan shellfish is their tropomyosin, a muscle protein, which elicits IgE binding in the sera of half or more of patients with shellfish allergies. It was first identified as the major allergen from shrimp and later recognized as a pan-allergen among invertebrate species including crustaceans and molluscan shellfish; e.g., squid, octopus, cuttlefish, mussels, scallops, and oysters. Although bivalves are likely to be the most frequently ingested class of molluscan shellfish, the existence of allergic reactions to bivalves is rather poorly documented in the medical literature. The prevalence of allergies to oysters, clams, mussels, scallops, and cockles has been reported in different countries, but these were mainly based on surveys without any diagnostic follow-up. However, evidence for the existence of mussel allergy is reasonably strong because of sensitivity to mussels by the presence of mussel-specific IgE in patient’s blood serum
[50][37]. Arginine kinase (AK) has more recently been identified as a novel allergen in
Crassostrea angulata. After cloning to produce recombinant AK (rAK), it was found that native AK and rAK had similar IgG/IgE-binding activities and physicochemical properties, and exhibited cross-reactivity among oysters, shrimps, and crabs after the serological analysis of oyster-sensitive individuals
[51][38].
The accumulation of metals and human pathogens by bivalves also provides an opportunity because bivalves tolerate these contaminants. Their immobility and wide distribution allow bivalves to be used for monitoring the concentration of such pollutants in coastal areas
[12][3]. They also remove contaminants by being hyperaccumulators of Cu (
Crassostrea virginica [2013 mg Cu kg
−1 ]), Pb (
Mytilus edulis [506 mg Pb kg
−1 ]), Cd (
Pinctada albina [108 mg Cd kg
−1 ]), and Al (
Crassostrea rhizophorae [2240 mg Al kg
−1 ]), and have approached this status for Zn (
Crassostrea virginica [9077 mg Zn kg
−1])
[11][2]. However, there is no information yet regarding the hyperaccumulation of heavy metals by
P. placenta. Similarly, with respect to human pathogens, allergens, and contaminants, there are no systematic data on the
P. placenta. The above considerations of other molluscs indicate that this is an area ripe for investigation.