This study describes morphological characteristics of pen shells collected along the coast of northern Iloilo, Philippines. A total of 380 pen shell individuals with intact shells and their adductor muscles were carefully examined and measured. Eleven species were studied, namely: Atrina pectinata (Linnaeus, 1767), Atrina inflata (Dillwyn, 1817), Atrina vexillum (Born, 1778), Atrina seminuda (Lamarck, 1819), Atrina rigida ([Lightfoot], 1786), Pinna bicolor Gmelin, 1791, Pinna atropurpurea Sowerby, 1825, Pinna deltodes Menke, 1843, Pinna muricata Linnaeus, 1758, Pinna incurva Gmelin, 1791, and Pinna nobilis Linnaeus, 1758. The species were identified based on the nine characteristics of the valve for the genus Pinna and eight for the genus Atrina. These characteristics were then correlated with their adductor muscles’ morphology. Analysis of variance revealed that the three most dominant species investigated under genus Atrina, namely Atrina pectinata, Atrina inflata, and Atrina vexillum, were found to be significantly different in the eight characters of the valve (P < 0.05). Moreover, three representative Pinna species, Pinna bicolor, Pinna atropurpurea, and Pinna deltodes, were significantly (P < 0.05) different based on shell width, dorsal posterior shell margin, sulcus width, and dorsal posterior margin to dorsal nacreous margin. The observed high correlation (P < 0.05) between adductor muscle properties and different shell length characteristics for five dominant species can be used as a predictor of growth and suggests that the increase in the size of adductor muscle correlates to the increase in the size of the mentioned shell characteristics. No previous study of this kind was conducted in the Philippines. This work provides relevant information for related biological research on other pen shell species and for the management of pen shell resources in northern Iloilo and, possibly, other regions in the world.

adductor muscle, Atrina pectinata, fisheries management, growth predictor, Pinna bicolor, taxonomy

The family Pinnidae (Order: Ostreida) belongs to the class Bivalvia and is commonly known as pen shell (Deudero et al. 2015). They are large, thin, wedge-shaped shells (Burns and Smith 2011) that are nearly burrowed in soft substrates in shallow waters. A total of 61 species is known worldwide (Deudero et al. 2015). In the Philippines, 15 species occur (Poppe 2010; Schultz and Huber 2013; Lemer et al. 2016), including four species in northern Iloilo (Laureta 2008).

Morphologically, pen shells are cryptic (Lemer et al. 2016) and are extremely prone to breakage, and this makes their identification confusing and challenging (Idris et al. 2008). Although they can repair their damaged shells by themselves, the repaired shells are always different from intact ones in form and sculpture (Rosewater 1982; Idris et al. 2008). Species of the genus Atrina have a continuous nacreous area that occupies the entire anterior inner valve surface (Rosewater 1982; Scheltema and Williams 1983). In contrast, species of the genus Pinna, another genus of the family Pinnidae, have a nacreous area that is divided into dorsal and ventral lobes by an anteroposteriorly directed sulcus (Souji et al. 2014).

Aside from northern Iloilo, other active fisheries for pen shells are localized in various areas in the Philippines, but the species of interest is always Atrina pectinata (Linnaeus, 1767) because of the high demand for its adductor muscle by the export market, particularly in Taiwan. Each year about 20 tonnes of this species are captured by local divers in the southwestern region of the Visayan Sea (Del Norte-Campos et al. 2021) while about 18 tonnes are gathered in the Province of Eastern Samar (Diocton and Adalla 2019). Meanwhile, the mantle of Atrina pectinata is consumed locally. Similar practices are noted in Sorsogon Province, in the southeastern region of the main island of Luzon (Amano and Mojados 2020). Pen shell fishery is a major activity in coastal areas throughout the Visayan Sea, but it is rarely documented. In this study area, which forms part of the Visayan Sea, a small number of poor fishers who are mostly educated only up to primary level, conduct gathering operations 20 days per month to support their households mainly from the sales of adductor muscles, but they also land various fin fish species and other bivalve species as bycatch (Jela unpublished¹). Due to the high economic value and food value of adductor muscles (Greenwald 1996; Katsanevakis et al. 2011; Leal-Soto et al. 2011; Basso et al. 2015), it is likely that demand for pen shells will continue to increase while a decline in production persists.

Pen shells have a large posterior adductor muscle that is responsible for the opening and closing of the shell. It appears as dark and light phases, which are respectively called blocking and working muscles (Czihak and Dierl 1961). It is the most important energy storage site in many marine bivalves and accumulates mostly protein and carbohydrate reserves to sustain gametogenesis (Saucedo and Southgate 2008). The age of the pen shell can be discerned through the scar created by the posterior adductor muscle (Garcia-March et al. 2011); however, it is difficult to count its early years because of the nacre deposition in later life that conceals the few scars that represent the year of life of the pen shell (Richardson et al. 2004).

In managing wild pen shell resources, it is important to make an accurate identification of species occurring in a certain locality. Previously, Laureta (2008) identified a total of four pen shells of the family Pinnidae in the Visayan Sea off the coasts of northern Iloilo. However, this count is likely low because the Visayan Sea is home to diverse bivalves. Moreover, a preliminary cursory investigation of adductor muscles that are sold in the market revealed varied shapes and forms, suggesting the occurrence of not just four species and that the pen shell fishery is no longer limited to Atrina pectinata. However, sorting of the adductor muscles to determine species is difficult because no information is known about the morphological characteristics of collected species of the family Pinnidae in the area.

Obtaining morphological data of pen shells at the landing sites is not possible due to the existing fishing method, which requires underwater extraction of the meat each time a pen shell is encountered. With the aid of a compressor, divers extract individual pen shells from their habitat, shuck all the meat, and leave empty shells at the sea bottom. This method is preferred because more meat can be collected during each dive. Moreover, the shells are no longer loaded on their small boats because of their bulkiness. Also, there is no motivation for landing the shells because there is no market for them. Therefore, categorization of species monitoring based on shell shape and size is not possible. However, it was observed that the adductor muscles landed at local markets with their mantle have different shapes. Thus, an alternative morphological characterization strategy based on the shapes of the adductor muscles can be adopted. The information obtained would provide insights as to which species need to be managed. More detailed measurements of their morphological characteristics would also provide information about pen shell diversity in the area.

This study focuses on species of the family Pinnidae. First, it aims to update the checklist of Atrina and Pinna species that occur in the coastal waters of the Visayan Sea, off northern Iloilo, in the Philippines. This information is useful for future research related to the taxonomy, morphology, and genetic diversity of pen shell species in the Philippines. The second objective seeks to determine some relations in the characters of landed adductor muscles and the pen shells, which may be used for identifying species for better management.

Study area. This study was carried out in the coastal waters of northern Iloilo, part of the Visayan Sea, Philippines (Fig. 1A). Pen shells were directly collected by fishers from the seabed during low tide; this corresponds to 0 m depth in our data sheet. Divers were contracted to collect pen shells also at water depths of 5, 10, 15, and 20 m, which were established at each of the designated six sampling stations where they reportedly occur (Fig. 1B).

Figure 1. 

Map of the Philippines showing the province of Iloilo, Philippines (A), and location of six sampling stations at five water depths (0 m, 5 m, 10 m, 15 m, and 20 m) (B) in the coastal waters of northern Iloilo, part of Visayan Sea, Philippines.

Sample collection and measurements. A total of 380 intact adult individuals of various pen shell species were collected using compressor diving, stored in a styrofoam box, preserved with ice, brought to the biological laboratory of Northern Iloilo State University, and carefully examined for morphological measurements and identification. The specimens were cleaned with a metal knife to remove epibionts and washed with tap water to remove dirt. Shells were carefully shucked individually and flesh was removed. The right valve of each shell was measured using a Vernier caliper to the nearest 0.01 mm following the method of Idris et al. (2008), with emphasis on the following parameters (distances): 1) total shell length (TSL); 2) length of anterior to posterior adductor margin (LAPAM); 3) posterior adductor to posterior shell margin (PAPSM); 4) dorsal posterior shell margin (DPSM); 5) dorsal margin (DM); 6) shell width (ShW); 7) sulcus width (SuW); 8) posterior adductor margin to posterior nacreous margin (PAMPNM); and, 9) dorsal nacreous length (DNL).

The measurements are not the same for all species because of varied morphologies. It is important to note that the dorsal posterior shell margin differs in Atrina and Pinna species. Measurement of nacreous length started at the end of the muscle scar because the nacreous layer was apparent at the end of the posterior margin of the anterior adductor muscle scar. Moreover, for species of the genus Pinna, the sulcus width was also measured (Fig. 2). The dorsal posterior shell margin of different species with different morphologies was identified by dividing the posterior margin into equal parts (dorsal and ventral margin). The dorsal posterior shell margin was then measured. The shell specimens were then photographed, labeled, and stored.

Figure 2. 

A diagram of the interior right valve of genus Pinna (A) showing the position of the nacreous layer and 8 characteristics of the shell. 1 = total shell length (TSL); 2 = length of anterior to posterior adductor margin (LAPAM); 3 = posterior adductor to posterior shell margin (PAPSM); 4 = dorsal posterior shell margin (DPSM); 5 = dorsal margin (DM); 6 = shell width (ShW); 7 = sulcus width (SuW); 8 = posterior adductor margin to posterior nacreous margin (PAMPNM) and 9 = dorsal nacreous length (DNL). A diagram of the interior right valve of genus Atrina (B) showing the position of the nacreous layer and 8 characteristics of the shell. 1 = total shell length (TSL); 2 = length of anterior to posterior adductor margin (LAPAM); 3 = posterior adductor to posterior shell margin (PAPSM); 4 = dorsal posterior shell margin (DPSM); 5 = dorsal margin (DM); 6 = shell width (ShW); 7 = posterior adductor margin to posterior nacreous margin (PAMPNM); and 8 = dorsal nacreous length (DNL).

Species identification. The specimens were identified based on their morphological characteristics such as shell structure, specifically in the way the parts are organized, and sculpture, as indicated by length, color patterns, and other related traits. Identification guides include the works of Grave (1911), Winckworth (1929), Butler and Keough (1981); Scheltema and Williams (1983); Poutiers (1998), Leal (2002), Idris et al. (2008), and Laureta (2008).

Data analysis. The mean and standard deviation of the different shell and adductor muscle morphometric characters were calculated for each species. One-way analysis of variance was used to estimate the differences in the means of the different parameters of the shells. Post-hoc tests were subsequently applied to show how the various parameters differed. This analysis was performed using the SPSS package, ver. 20. Before analysis, the normality of data was tested using the Kolmogorov–Smirnov test. Using three dominant species of the two pen shell genera in this study, the relation between shell and adductor muscle morphology was determined by linear regression.

Five species of the genus Atrina, namely, Atrina pectinata, Atrina inflata (Dillwyn, 1817), Atrina vexillum (Born, 1778), Atrina seminuda (Lamarck, 1819), and Atrina rigida ([Lightfoot], 1786) and six species of the genus Pinna, namely, Pinna bicolor Gmelin, 1791, Pinna atropurpurea Sowerby, 1825, Pinna deltodes Menke, 1843, Pinna muricata Linnaeus, 1758, Pinna incurva Gmelin, 1791, and Pinna nobilis Linnaeus, 1758 were collected from the waters of northern Iloilo. Table 1 summarizes the measurements of shell characteristics of the samples collected while Table 2 provides descriptive characteristics of those species. Figures 3, 4 show the images of the shells of these species. The dominant species were A. pectinata, A. inflata, A. vexillum, P. bicolor, P. atropurpurea, and P. deltodes.

Figure 3. 

Photographs of selected species of the genus Atrina showing the external and internal surface of the right valve collected from northern Iloilo, Philippines. External valve (A.1, B.1, C.1, D.1, E.1), internal valve (A.2, B.2, C.2, D.2, E.2). Atrina pectinata (A.1–A.2), A. vexillum (B.1–B.2), A. inflata (C.1–C.2), A. seminuda (D.1–D.2), and A. rigida (E.1–E.2).

Figure 4. 

Photographs of selected species of the genus Pinna showing the external and internal surface of the right valve collected from northern Iloilo, Philippines. External valve (A.1, B.1, C.1, D.1, E.1, F.1), internal valve (A.2, B.2, C.2, D.2, E.2, F.2). Pinna bicolor (A.1–A.2), P. deltodes (B.1–B.2), P. atropurpurea (C.1–C.2), P. incurva (D.1–D.2), P. nobilis (E.1–E.2), and P. muricata (F.1–F.2).

Differences in shell morphology of dominant species. Only the dominant species were used to compare the shell morphology of pen shell species. These include three species of the genus Atrina, namely, A. pectinata, A. inflata, and A. vexillum, and three species of the genus Pinna, namely, P. bicolor, P. deltodes, and P. atropurpurea. These were subjected to length–length analysis. The other species were not analyzed because the number of specimens for them was inadequate. Figure 5 presents eight morphometric measurements of the three dominant Atrina species. They were significantly different in all the characteristics measured in this study (ANOVA, P < 0.05). Post-hoc analyses revealed that the total shell length, length of posterior adductor to posterior shell margin, dorsal margin, and dorsal nacreous length of A. pectinata was always significantly higher (P < 0.05) than their corresponding values in A. vexillum and A. inflata. The length of its anterior to posterior adductor margin was significantly different relative to A. inflata (P < 0.05) but was similar to A. vexillum. Only A. pectinata and A. inflata differed in terms of the dorsal posterior shell margin (P < 0.05). The shell width of A. pectinata was significantly lower than A. vexillum (P < 0.05) but not different from A. inflata. And, the posterior adductor margin to the posterior nacreous margin of A. pectinata was significantly higher compared to A. inflata and A. vexillum due to the 0 value of the posterior adductor margin to posterior nacreous margin of A. vexillum (P < 0.05). Meanwhile, Figure 6 shows the morphometric characteristics of the three dominant Pinna species. These species differed based on the dorsal posterior shell margin, the width of the shell, the sulcus width, and the posterior adductor margin to the posterior nacreous margin (ANOVA, P < 0.05). The three species differed only in several characteristics. The dorsal posterior shell margin of P. deltodes was significantly higher than those of P. atropurpurea and P. bicolor, but P. atropurpurea and P. bicolor also differed (P < 0.05). The shell width of P. bicolor was significantly different (P < 0.05) relative to P. deltodes and P. atropurpurea, which were similar. The three species had different sulcus widths (P < 0.05). The posterior adductor margin to the posterior nacreous margin of P. bicolor was significantly lower (P < 0.05) than those of P. atropurpurea and P. deltodes, which were similar.

Figure 5. 

Measurements of eight morphometric characters of Atrina inflata (n = 45), A. pectinata (n = 231), and A. vexillum (n = 17). Values are expressed as the mean ± standard deviation. TSL = total shell length (A), LAPAM = length of anterior to posterior adductor margin (B), PAPSM = posterior adductor to posterior shell margin (C), DPSM = dorsal posterior shell margin (D), DM = dorsal margin (E), ShW = shell width (F), PAMPNM = posterior adductor margin to posterior nacreous margin (G), DNL = dorsal nacreous length (H). Small letters above the columns indicate the results of post-hoc tests.

Figure 6. 

Measurements of nine morphometric characters of the genus Pinna: P. bicolor (n = 43), P. atropurpurea (n = 34), and P. deltodes (n = 10). Values are expressed as the mean ± standard deviation. TSL = total shell length (A), LAPAM = length of anterior to posterior adductor margin (B), LPAPSM = length of posterior adductor to posterior shell margin (C), LDPSM = length of dorsal posterior shell margin (D), DM = dorsal margin (E), ShW = shell width (F), SuW = sulcus width (G), PAMPNM = posterior adductor margin to posterior nacreous margin (H), DNL = dorsal nacreous length (I). Small letters above the columns indicate the results of post-hoc tests.

Adductor muscle morphology. Representative specimens of the posterior adductor muscles of the most dominant species belonging to the genera Atrina (Fig. 7) and Pinna (Fig. 8) are illustrated for comparison. Table 3 presents additional information about the adductor muscles of the five dominant species examined.

Figure 7. 

Photographed images of the posterior adductor muscles of Atrina pectina (A, B, C), Atrina inflata (D, E, F), and Atrina vexillum (G, H, I) collected from northern Iloilo, Philippines.

Figure 8. 

Photographed images of the adductor muscle of Pinna bicolor (A, B, C), Pinna atropurpurea (D, E, F), and Pinna deltodes (G, H, I) collected from northern Iloilo, Philippines.

Relation between shell length characters and adductor muscles of dominant species. The regression equations between the different length characteristics and their respective adductor length and thickness for five dominant pen shell species (r², 0.23–0.94) are shown in Table 4. This procedure was not performed on P. deltodes because the number of samples was inadequate. All eight length characteristics of A. pectinata and A. inflata were all positively significantly correlated (P < 0.05) with their adductor muscle length and thickness. In the case of A. vexillum, dorsal nacreous length (DNL) was not correlated with its adductor muscle thickness, whereas DNL and dorsal margin were not correlated with its adductor muscle length. Meanwhile, all nine shell length characteristics of P. bicolor were positively correlated with its adductor muscle thickness (r², 0.59–0.88) and length (r², 0.47–70). The shell length characteristics of P. atropurpurea were also positively correlated with its adductor muscle thickness (r², 0.40–0.84) and length (r², 0.38–0.84). The total shell length and adductor muscle thickness of P. bicolor and P. atropurpurea exhibited a high correlation (r² = 0.88 and r² = 0.84, respectively P < 0.05). (Table 4).

Species of the family Pinnidae are cryptic and can easily adapt to environmental changes (Lemer et al. 2014). The results of the presently reported study revealed that they indeed differ in size, structure, and color. These characteristics can be confusing, especially for early career scientists, as their shells can easily be broken (Idris et al. 2008). Although it is already known that the presence of a longitudinal sulcus separating the dorsal and ventral lobes of the nacreous layer in species of the genus Pinna distinguishes them from species of the genus Atrina (see Rosewater 1982), the possible presence of species not previously recorded in this area is still worth investigating.

Five species of the genus Atrina and six species of the genus Pinna representing the family Pinnidae were identified. The number of identified species updates the previous record for this area (Laureta 2008). A comprehensive presentation of the differences in shell morphology of the most abundant species, A. pectinata, A. inflata, A. vexillum, P. bicolor, P. atropurpurea, and P. deltodes, is believed to be the first attempt for these species, which may be useful later for comparative studies when new records are made.

The ecological conditions of the coastal habitats in northern Iloilo apparently define the pen shell species that dominate in an area. For example, many of the six species investigated are different from other areas where pen shells are known to thrive, such as in Sugai Pulai, Malaysia (Idris et al. 2008). The single specimen of P. nobilis, which was previously noted to be the largest pen shell species recorded (Basso et al. 2015) and reportedly most dominant in the Mediterranean Sea (Zavodnik et al. 1991; Richardson et al. 1999; Cappello et al. 2019), was also the largest among all the pen shells collected at this study site. Other species that occurred only once, namely, A. seminuda, A. rigida, and P. incurva, are recorded for the first time in this area; this information is important to note because it can be used to make ecological reports about pen shell diversity in northern Iloilo and can be included in the management plan for these resources. There are now 11 species compared to the previous record for this area (Laureta 2008), and four of these were observed to be rarely occurring (see Tables 1, 2, 3). This strongly suggests that there may still be unrecorded species that could be discovered if a more comprehensive survey covering a larger area including deeper waters is made. This may be the subject of a more comprehensive study worth considering in the future.

The analysis of pen shell morphology relied on nine internal and external characteristics of the valve among species of the genus Pinna and eight characteristics among species of the genus Atrina. The external surface sculpture of the valves and the size and position of the adductor muscles, which create distinctive scars on the inner side of the valves, were used to define individual species of the family Pinnidae, as suggested by Rosewater (1961). The comparisons made revealed that the three Pinna species, P. bicolor, P. atropurpurea, and P. deltodes, were found to be different based on shell width, dorsal posterior shell margin, sulcus width, and dorsal posterior margin to dorsal nacreous margin, similar to the study of Idris et al. (2008). The differences of the adductor muscle scar from the posterior nacreous margin appeared to be influenced by the different positions of the muscle within the shell. Meanwhile, the difference in the length of the dorsal margin was due to the different curvatures of their shell.

Although no new species were identified in this study, following this comprehensive examination of specimens collected with a more comprehensive survey will lead to the generation of a comprehensive checklist of pen shell species in northern Iloilo. The application of this same method to other known pen shell-occurring areas in the Philippines, such as in the Samar Sea, where an active fishery exists (Diocton and Adalla 2019), may also be worth considering.

The considerable size of the adductor muscle and its nutritional value (Wu and Wu 2017) make pen shells of great interest to fisheries. It serves as a source of income (Diocton and Adalla 2019; Del Norte-Campos et al. 2021) and food (Greenwald 1996) for many artisanal fishers. However, in northern Iloilo, only adductor muscles are landed and sold in the market, leaving empty shells scattered in the substrate. This practice by fishers presents challenges in assessing the state of pen shell populations in the area or the management of these resources unless strategies to regulate the resources are introduced soon. Under such conditions, these resources may be overexploited, just like most wild fishery resources (Pauly et al. 1998).

It is important to note that no previous characterization of the adductor muscle was made for pen shells, and the use of this information may give previously unexplored insights about these resources. The linear regression analyses and correlations made with various shell length parameters with adductor muscle thickness and length may enable fishery scientists to determine the impacts of pen shell fisheries on the resources more precisely by closely monitoring the adductor muscles that are sold in the market, but this would even be more realistic if smaller-sized individuals are also represented. With the expected depletion of pen shell resources as harvesting pressure increases, pen shell juveniles may be harvested and secretly sold or brought home for domestic consumption. Perhaps, it is important to include size limitation measures among the strategies to regulate the harvesting of pen shells to ensure the sustainability of this important resource in the area.

Based on the different forms of the marketed adductor muscles, it is evident that species other than A. pectinata, which commands the highest value among all pen shell species, are also accepted for general consumption. The linear regression analyses and correlations between various shell characters and several adductor characters of the six dominant species were done to infer the state of wild pen shell populations. Through this, it is evident that certain characteristics can be used to discriminate the different species under Pinna. The appropriate procedure to do this is to relate the dimensions of the adductor muscles with various characteristics of their shells. Using extracted information from the dominant species, it seems possible to determine the species of their source organisms.

The described and analyzed morphological characteristics of the adductor muscle of A. pectinata, A. inflata, A. vexillum, P. bicolor, and P. atropurpurea suggest that the relations of thickness and length of adductor muscles with the various lengths characters of the shell can be used to differentiate the species by looking at the characteristics of the adductor muscles. The high correlations between various adductor muscle characteristics and shell length characters indicate that they could be a good for taxonomic purposes. The specific and distinct identity of each species in this study has provided information on the diversity of pen shells as well as an opportunity for the newly discovered species to be included in the catalog of bivalves in northern Iloilo, Philippines. Also, through the marketed adductor muscles, it is possible to assess the level of pressure posed by fishers on wild pen shells in this area using established modeling methods. Thus, this study may be useful in stock assessment and in monitoring the sizes of shucked pen shells.

This study is part of the dissertation of the first author, who is a scholar under the Advanced Science and Technology Human Resource Development (ASTHRD) Program of the Department of Science and Technology (DOST). The conduct of her field research was partially supported by “Marine Fisheries Assessment of Panay: Building Local Fisheries Information through Research Capability Enhancement in HEI’s”, a research project that was supported by the Commission on Higher Education (CHED). Permits to conduct the study were granted and additional supporting data were provided by the Municipal Mayors of Carles, Estancia, and Batad, all in Iloilo Province.