History and Prospects for the Sustainability and Circularity of the Windowpane Oyster Placuna placenta Fishery in the Philippines

Round 1

Reviewer 1 Report

This manuscript draws together some information on the management, meat quality, catches, and uses over time of windowpane oysters in the Philippines. Much of the material was new to me, so that suggests the value of placing this information in a single review publication. My comments address that there are certain parts of the manuscript that seem too general for a review of this species, and the advantage of adding other details about the species that are likely known.

Abstract: “highlights that these also…” Needs to be rewritten because the antecedent for “these” is unclear. Do you mean, “Because other marine molluscs contain pharmaceuticals, the windowpane oyster might also serve as a source of such high-value products”. If this is what you mean, then I’m not convinced that the claim is of sufficient certainty to be included in the abstract.

Bottom of page 3: uncertain what time period is involved in setting the allowable size limit and need for a license

Top of p 4: “quaint medicines” use another term other than “quaint”

Generally the sections on life history, and bioactive compounds sound like encyclopedia reviews of broader taxonomic groups, rather than specific to this species. Especially sections 4.1.1, 4.1.2, and 4.1.3 state only that Placuna placenta has not been studied, which seems inappropriate for a review. The paragraph at the end of section 4 would suffice, if a few references were added there.

What is specific to this species?

Unusual shell – needs description of its chemical composition (probably not just calcium carbonate). Needs clearer description of the life stages, and the size and estimated age at which the shell is useful. (page 2)

Exploitation timeline – You can make the section on reported historical catches easier to understand in terms of trends, or create a time series graph. (page 5)

Mucus – mucus could be a deterrent to use of the meat as food, therefore worthy of mention in the abstract. The first mention of difficulties with the meat is out of context. (heating and purifying for 3 days, top of p. 4)

Nutritional value – it’s wonderful to have data on the chemical content of the meat of P. placenta and several other species in Tables 1-3. Can you add numbers referring to the variation around the mean values, so it is easier to tell if P. placenta differs from other species? Also, given its relatively low moisture content for a bivalve, that would lead to relatively high levels of compounds per wet mass (as in Tables 2 and 3). Discuss, or modify tables per dry mass. Also, I suggest placing P. placenta as the first row of each table, otherwise it’s hard to pick out.

Management –end of page 5 and beginning of page 6 have statements about some management, culturing, and outplant efforts, but insufficient detail to understand the efficacy of these efforts. Slightly more detail in this section would help support your claim that management efforts need to be at larger scales.

“Restoration of the oyster beds” is mentioned in the conclusion, but there was no earlier description of these beds (only a general description of how bivalves can clean the water as it sweeps across beds). At what depths and on what substrates are P. placenta found, and how dense do they get in “beds”?

Check spelling of bivalve throughout. A couple of places have repeated words or words out of order.

Author Response

Reviewer 1

1. “This manuscript draws together some information on the management, meat quality, catches, and uses over time of windowpane oysters in the Philippines. Much of the material was new to me, so that suggests the value of placing this information in a single review publication. My comments address that there are certain parts of the manuscript that seem too general for a review of this species, and the advantage of adding other details about the species that are likely known.”

Author response

There is not that much known about P placenta – indeed many past reviews have largely summarised points from Hornell’s work. It is common that marine organisms of economic and ecological importance in the Global South are grossly understudied. As the reviewer states bringing what we know into one review has considerable value. Regarding sections where we review, e.g., ‘Bioactive compounds’, so Sections 4.1.1-4.1.3, this is a limited summary of what is known, but it does point the reader to the potential. We feel this is important. As we state in the Abstract and elsewhere, research into this potential is necessary to establish what is realisable. Our motivation is that readership will extend beyond researchers to stakeholders. Being able to provide an executive summary with a single point of reference is unfortunately often more effective with, e.g., government and policy making stakeholders, than an executive summary with many references. This is one of the ‘functions’ of the review and why we included such information, with references to the detailed analyses others have performed.

2. “Abstract: “highlights that these also…” Needs to be rewritten because the antecedent for “these” is unclear. Do you mean, “Because other marine molluscs contain pharmaceuticals, the windowpane oyster might also serve as a source of such high-value products”. If this is what you mean, then I’m not convinced that the claim is of sufficient certainty to be included in the abstract.”

Author response

The confusion arises due to ‘also’ and not specifying the absence of knowledge. This has been corrected to:

“Research on other molluscs and marine organisms highlights that these contain high value pharmaceutical products, an unexplored facet of windowpane oysters.”

3. “Bottom of page 3: uncertain what time period is involved in setting the allowable size limit and need for a license”

Author response

Unfortunately such details were not recorded when the information was acquired over a Century ago. What we have in the historical record is that this was regulated by the village chief, as follows  (units converted to SI). Below is a copy of the information available to us:

“Section 2. Issuance of permit. - It shall be unlawful for any person to gather, take, remove or collect "kapis" in Philippine waters without a permit duly issued by the Director or his duly authorized representative. Section 3. Prohibition. - The gathering, taking, removing or collecting of kapis less than 80 millimeters in diameter measured from the base perpendicular towards the top edge of the shell, and the use of mechanical rakes and dredges, or the use thereof on board a motorized boat are hereby prohibited.”

The text (now top of page 4) has been altered as follows:

“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 validity is not recorded)”

4. “Top of p 4: “quaint medicines” use another term other than “quaint””

Author response

We have used the term ‘folk’ instead, which is more appropriate.

5. “Generally the sections on life history, and bioactive compounds sound like encyclopedia reviews of broader taxonomic groups, rather than specific to this species. Especially sections 4.1.1, 4.1.2, and 4.1.3 state only that Placuna placenta has not been studied, which seems inappropriate for a review. The paragraph at the end of section 4 would suffice, if a few references were added there.”

Author response

As noted above, we feel that a brief overview of the potential is important in terms of the strategic ambitions of the review, which includes encouraging government stakeholders and policy makers to support the necessary future research. As these sections are short and information dense by means of extensive references, we feel their value to the wider community supports their retention. As an aside, one should note that this is merely a very small selection of the research output in this area and that a comprehensive review of the state-of-the-art of this exciting field here or in ‘Marine Drugs’ is well overdue.

6. “What is specific to this species?”

Author response

Assuming this refers to the above, there are no data, which is why we fell it is useful to highlight that marine organism contain a wealth of potential high value compounds and provide a little background on what seem likely to be the ones with the highest commercial potential.

7. Unusual shell – needs description of its chemical composition (probably not just calcium carbonate). Needs clearer description of the life stages, and the size and estimated age at which the shell is useful. (page 2)

Author response

We have now included reference to a recent materials science analysis on the P. placenta shell. There is as yet no comprehensive ‘omics description of the biomolecular components of the shell, let alone an analysis of the structural assembly at the atomic level.

New text page 2 “In younger specimens, the shell is secured by a V-shaped ligament, is thin and more or less translucent, becoming opaque with age and so has been considered to be ‘mica-like’ [7]. However, recent detailed physical analysis demonstrates that the shell is 98.9 ± 0.1 calcite (calcium carbonate) and allows transmission of 80 % of visible light [8]. Its thinness does not compromise its strength, by virtue of combining discrete biomolecular structures (composition and atomic structure unknown) within the calcite. In general the oysters are harvested from 18 months, when the shell is ≥80 mm in diameter.”

8. Exploitation timeline – You can make the section on reported historical catches easier to understand in terms of trends, or create a time series graph. (page 5)

We have simplified the text to provide the reader with a clearer view of trends:

“The result is a documented decline in harvest and revenue, recorded locally and nationally.

Locally in Bataan, based on the records of the Bataan provincial Agriculturist’ Office in 2016, 248 tonnes of windowpane oysters were harvested and there was a reduction in harvest of the shellfish to 154 tonnes in 2017 and to 138 tonnes in 2018, so a 45 % decline in just two years. The same scenario is repeated across all regions of the Philippines where windowpane oysters are harvested. Thus, 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 [2,20–22]. Consequently, the export of windowpane oyster products, which had an important economic impact in 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 [23,23,23], it declined (USD 7.15 million in 1994 [22], USD 4.45 million in 1996 [21]) to USD 1.085 million in 2021 [2].”

9. Mucus – mucus could be a deterrent to use of the meat as food, therefore worthy of mention in the abstract. The first mention of difficulties with the meat is out of context. (heating and purifying for 3 days, top of p. 4)

Author response

Some confusion has arisen due to poor wording. The statement

“Badjao women and children shucked the shells, and slowly heated and purified the flesh for 3 days.’

In fact refers to the method used to obtain and clean the pearls and has nothing to do with the preparation of the meat.

The text at the top of P 4 has been altered to reflect this:

“Badjao women and children shucked the shells, and pearls were obtained by slowly heating the meat over 3 days.”

As for preparing the meat as a food, there is no historical information available on the consumption of the meat and information on processing the meat (Section 4.2 page 12) derives from modern times.

Thus, the mucus does not figure here. However, as mucus is primarily polysaccharide and there are many uses of polysaccharides in home and personal care products as well as in medicine, this is one of our motivations for delving into this general area in Section 4, though of course the composition of the P. placenta mucus is not known.

We have, therefore, added some text at the bottom of page 3 to highlight the extensive mucus in P. placenta early in the review and the fact it is easily removed by washing with water, which is current practice in preparing the meat.

“Windowpane oyster meat is edible, though the oyster has unusually extensive mucus, well above the small amount used to produce pseudo feces in other molluscs. This mucus is simply removed by washing when preparing the meat  (Section 4.1.2).”

The process describe at the top of Page 4 relates to the preparation of the shell, not the meat. This point is clarified by adding ‘These’ to the second sentence to the text:

“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].”

The process of heating etc. to prepare the pearls describes that employed by the Badjao divers over a century ago. It is thus a historical process used and the text has been clarified on this point by reinforcing the point in the paragraph that the information refers to a historical/traditional process.

“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 validity is not recorded)”

10. Nutritional value – it’s wonderful to have data on the chemical content of the meat of P. placenta and several other species in Tables 1-3. Can you add numbers referring to the variation around the mean values, so it is easier to tell if P. placenta differs from other species? Also, given its relatively low moisture content for a bivalve, that would lead to relatively high levels of compounds per wet mass (as in Tables 2 and 3). Discuss, or modify tables per dry mass. Also, I suggest placing P. placenta as the first row of each table, otherwise it’s hard to pick out.

Author response

The data presented are those extracted from the references. There is information for some species on variation, including seasonal variation.  However, the data on P placenta are limited, they are only by wet weight, there are no data available on a dry weight basis, of variation, either of technical replicate sor of  biological replicates, let alone seasonal variability. These are very important points so we have modified the text to further stress that improved data analysis would represent a major step forwards and we hope to convince stakeholders to adopt better practice in the future. We have moved the P. placenta data to the top row as suggested. So as not to overload the Table and text we point the reader to the references to find more in-depth data on the other species.

Page 6 new sentences:

  “Data in Tables 1-3 are reported in relation to wet weight, as there are no dry weight data for P. placenta). Whereas data on other species can include measurement in terms of dry weight, and of technical variation (multiple measurements on one sample), biological variation (multiple measurements on different biological samples) and seasonal variation, such information is not available for P. placenta and are omitted for the other species for the sake of clarity.”

11. Management –end of page 5 and beginning of page 6 have statements about some management, culturing, and outplant efforts, but insufficient detail to understand the efficacy of these efforts. Slightly more detail in this section would help support your claim that management efforts need to be at larger scales.

Author response

The information available is a range of case/ anecdotal reports in newspapers, pilot studies and government documents. Unfortunately, even the latter lack serious quantification. So there are a range of rules, but no information on enforcement or on the effect of rules/enforcement or on necessary longitudinal follow up. We now make this point in the text to stress the importance of the need for stronger data prior to embarking on better management practice.

New text bottom p6-top p6

“A combination of legal and remdial measures have been taken to try to reverse the decline of the P. placuna 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. placuna and much activity is devolved, for practice and implementation by concerned institutions and fisheries agencies according to their program 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 explains in part the continued decline of P. placuna harvests [24].”

New text bottom p 6

“There are limited data on the efficacy of restocking, notably in the Panay Gulf beds. In 1999 it was confirmed windowpane oyster juveniles were observed within a year. 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 bouys [29]. 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 and enforcement 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. “Restoration of the oyster beds” is mentioned in the conclusion, but there was no earlier description of these beds (only a general description of how bivalves can clean the water as it sweeps across beds). At what depths and on what substrates are P. placenta found, and how dense do they get in “beds”?

Author response

We have clarified the text, by including the term ‘oyster bed’ in the description of the natural history of the windowpane oyster at the bottom of page 3. As the next paragraph deals with depth and substrate, this should now be clear. Regarding density, there are no quantitative data relating to virgin oyster beds, as all have been subjected to extensive harvesting for many decades and no substantial oyster beds exist in marine reserves.

“The specific gravity of water in P. placuna oyster beds ranges from 1.019 g/mL to 1.015 g/mL at temperatures ~30.5 °C to 32 °C.”

Comments on the Quality of English Language

“Check spelling of bivalve throughout. A couple of places have repeated words or words out of order. “

Typos have been corrected.

Reviewer 2 Report

The paper needs some corrections. I put my suggestions in text.

Comments for author File: Comments.pdf

Author Response

Reviewer 2

Comments were highlighted in the PDF

1. Highlighted in the title, applicable to rest of text: Windowpane oyster/P placenta.

We have used the systematic name throughout rather than the trivial name.

2. Page 2, space after % - typo corrected.

3. Page 3, use of personal pronoun. Though historically the personal pronoun was used extensively in papers, is generally the case that papers nowadays are written impersonally and avoid personal pronouns. However, it is common to retain the use of the personal pronoun in describing the strategy of the experimental design, or the strategy that underlies a review. For this reason, we feel that the ‘we’ should be maintained here, as it provides an opportunity to ‘talk’ directly to the reader with respect to the underlying strategic aim of the review.

4. Tables 1, 2, 3

Crassostrea madrasensis has been corrected to Magallana bilineata.

The spelling of Cypraeidae is now corrected.

5. Table 4, commas removed

6. Page 9 the second ‘albina’ deleted

7. Page 11, two species names corrected and the second instance of “anodonta’ deleted.

Reviewer 3 Report

I found this to be a nice and thorough review of the windowpane oyster, fisheries in general, and conclusions about the potential for this as a culture product.

There are some instances within the manuscript that have some grammar or spelling issues, but overall, I felt the quality of English was fine.

Author Response

Reviewer 3

We have checked the text for typos and grammar. It is worth noting that UK spelling is used throughout, which may account for the perception of spelling errors.