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Ecology of Pinnidae (Mollusca: Bivalvia) from the Gulf of Thailand
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Cheewarat PRINTRAKOON1, *, Peter D ROOPNARINE2, Thamasak YEEMIN3
Acta Oceanologica Sinica | 2019, 38(2) : 52 - 69
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Acta Oceanologica Sinica | 2019, 38(2): 52-69
• Marine Biology •
Ecology of Pinnidae (Mollusca: Bivalvia) from the Gulf of Thailand
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Cheewarat PRINTRAKOON1, *, Peter D ROOPNARINE2, Thamasak YEEMIN3
Affiliations
  • 1 Animal Systematic Special Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
  • 2 Department of Invertebrate Zoology and Geology, California Academy of Sciences, San Francisco, California 94118, USA
  • 3 Department of Biology, Faculty of Science, Ramkhamhaeng University, Bangkok 10240, Thailand
Published: 2019-02-25 doi: 10.1007/s13131-018-1230-4
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The ecology of the family Pinnidae was studied by sampling three pinnid species from 36 sampling sites across four different microhabitats in the Gulf of Thailand. The species spatial distributions were mostly uniform, with some populations having random distributions. Species abundances differed between sandy and coral habitats according to non-metric multi-dimension scaling analyses. Although the Gulf of Thailand is a relatively small geographic area, habitats are varied enough to provide variable shell densities. Small islands are important distribution areas, and coral reefs provide both direct and indirect shelter which support high abundances, densities and increased shell size. The highest density was recorded in sand beds within coral reefs. Low density and small shell size in sand beaches might be related to high mortality in shallow water or to adaptations for survival in shallow waters. A clear correlation between sediment composition and species abundance was found in Pinna atropurpurea; abundance increased with the sand content of the sediment. For P. deltodes, abundance increased as the rock fraction of the sediment increased. These results suggest that adaptations in Pinnidae, such as shell size, shell morphology, and the exposure of the shell above the sediment-water interface, are responses for survival in different habitats.

density  /  distribution  /  pinnid shell  /  shell adaptation  /  the Gulf of Thailand
Cheewarat PRINTRAKOON, Peter D ROOPNARINE, Thamasak YEEMIN. Ecology of Pinnidae (Mollusca: Bivalvia) from the Gulf of Thailand[J]. Acta Oceanologica Sinica, 2019 , 38 (2) : 52 -69 . DOI: 10.1007/s13131-018-1230-4
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1 Introduction
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The Gulf of Thailand hosts a diverse array of shallow marine habitats, including nearshore coral reefs, mangrove forests and seagrass beds, which play an essential role in commercial harvesting of fish, molluscs and crustaceans (Office of Natural Resources and Environment Policy and Planning, 2004). Species of the bivalve molluscan family Pinnidae are distributed throughout the gulf and among these habitats. There are about 55 known species of recent pinnid species in the world (Schultz and Huber, 2013), concentrated mostly in tropical regions, including the Indo-Pacific, Indo-west Pacific (Rosewater, 1961; Morris and Purchon, 1981; Purchon and Purchon, 1981; Idris et al., 2008, 2011; Xue et al., 2012; Schultz and Huber, 2013), Australia (Butler and Keough, 1981; Butler, 1987; Beer and Southgate, 2006; Macreadic et al., 2014), Mediterranean (Richardson et al., 1999; Šiletić and Peharda, 2003; Katsanevakis, 2006; Coppa et al., 2010; Nebot-Colomer et al., 2016), tropical American waters (Turner and Rosewater, 1958) and Mexico (Cendejas et al., 1985; Arizpe, 1995). Two genera have been described from the Gulf of Thailand, Pinna Linnaeus and Atrina Gray, 1842. Both are harvested commercially in most regions for consumption of the large posterior adductor muscle (Rosewater, 1961; Nielson, 1976; Amornjaruchit, 1988; Swennen et al., 2001; Yu et al., 2004), known locally as “hoi jorb” or “hoi song ploo”. No study to date, however, has examined ecological properties of pinnid distribution in Thailand, which is essential for both evaluating the conservation status of the species, and potentially improving the fisheries productivity and sustainability. The main objective of this study is to provide an initial ecological baseline of Pinnidae in Thailand, including species densities, habitats and distribution, and dead shell proportions. We also report on individual masses, state of the byssal threads, and nature and size of particles to which individuals are attached.
Few data are available regarding the distribution and ecology of Pinnidae in Thailand. Most data are literature reports and checklists. For example, Amornjaruchit (1988) surveyed markets and interviewed villagers in the 22 coastal provinces of Thailand for economically important molluscan shellfish. Three species of Pinnidae were recorded: Pinna bicolor Gmelin, 1791, Atrina vexillum Von Born, 1778 and A. pectinata Linnaeus, 1767. These species are commonly recorded from the Gulf of Thailand, in particular the eastern region (Kurozumi et al., 1989; Sanpanich, 2011). Swennen et al. (2001) listed five pinnid species from the southern Gulf of Thailand; two Pinna species, P. bicolor Gmelin, 1791 as uncommon in the Pattani Bay, in seagrass beds at depth of 0.5 to 1 m below low tide level, and P. incurve Gmelin, 1791, common amongst catches of fishing boats off Pak Bang and Saiburi. Three species of Atrina were listed, A. inflata Dillwyn, 1817, A. lamelata Habe, 1961 and A. vexillum, in depths ranging from 12 to 22 m, near Pattani. Rosewater (1961) previously assigned all three species to the single species A. vexillum. Nielson (1976) listed P. bicolor and A. vexillum among 91 bivalves species recorded at the Phuket Marine Biological Centre, informing the pinnids as inhabiting shale patches on sandy beaches, and the reef flat. Tantanasiriwong (1979) also presented a checklist of Pinnidae among littoral and sublittoral marine bivalve mollusks from Phuket. Pinna bicolor was collected from muddy sand between tide marks, down to a depth of 8 m, whereas A. pectinata Linnaeus, 1767 and A. vexillum were record as embedded in sand landward of coral reefs. Carr (1991) recorded P. bicolor in depths of 0–5 m from the Phang Nga Bay, east of the Phuket Island. Recently, Silina (2012) reported that local variation of factors such as seasonal temperature, salinity and sediment load clearly influence the growth and longevity of A. vexillum in the southern gulf. Schultz and Huber (2013) reported up to ten pinnid species distributed in Thailand, including P. attenuata Reeve, 1858, P. incurve, P. atropurpurea Sowerby I, 1825, P. muricata Linnaeus, 1758, A. vexillum, A. chinensis Deshayes in Cuvier, 1841, A. exusta Gmelin, 1791, A. inflata, A. pectinata, A. penna Reeve, 1858 and Streptopinna saccata Linnaeus, 1758.
Pinnid bivalves generally have large fragile fan shaped valves, with umbones pointed and situated at the extreme anterior end of the shell. The posterior end of the shell is wide and gaping, reflecting the asymmetry of the adductor muscles, where the anterior muscle is generally much smaller than the posterior (Swennen et al., 2001; Schultz and Huber, 2013). Species range from the intertidal to subtidal, and may be found variously buried partially in sand, mud or gravel substrates, or attached to submerged hard substrates by a thick, silky byssus (Abbott and Dance, 2000; Schultz and Huber, 2013). The genera Pinna and Atrina can be distinguished easily, with Pinna having a nacreous layer on the valve’s interior, divided by a sulcus into dorsal and ventral lobes, whereas Atrina has a nacreous layer not divided into two parts (Swennen et al., 2001). Here we report on both the ecology of the pinnid species, P. atropurpurea, P. deltodes and A. vexillum in the Gulf of Thailand, and compare the intergeneric ecologies of Pinna and Atrina.
2 Materials and methods
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2.1 Study area
Pinnid species were studied in three areas of the Gulf of Thailand, referred to different municipal and territorial waters (Office of Natural Resources and Environment Policy and Planning, 2004), and specimens were collected from six zones (Fig. 1). The first zone is the innermost region of the upper Gulf of Thailand including the Sichang Island (Zone A; 1–3): Ngo Cape (13°07′54.98″N, 100°48′57.27″E), Hintasin (13°07′55.56″N, 100°49′5.10″E) and Randokmai Island (13°09′6.00″N, 100°50′2.65″E) (Fig. 1A); and the Lan Island (Zone B; 4–6): Sak Island (12°56′45.64″N, 100°47′25.77″E), Yuon Cape (12°54′49.13″N, 100°47′12.23″E), Tharai Bay (12°54′33.72″N, 100°47′01.81″E) (Fig. 1B) of Chonburi Province.
The second zone (Zone C and D) are the two islands of Trat Province at the eastern end of the upper Gulf of Thailand including Changnoi Island (7 and 8): western coast of Changnoi (12°09′31.71″N, 102°14′42.92″E) and eastern coast of Changnoi (12°09′41.00″N, 102°14′58.90″E), and the Chang Island (9): Sabbarot Bay (12°08′36.99″N, 102°17′10.11″E) (Fig. 1C); and the Kood Island (10–12): Sai Bay (11°38′28.02″N, 102°36′41.53″E), Kluai Bay (11°41′09.17″N, 102°36′19.94″E) and Praw Bay (11°35′29.0″N, 102°33′30.4″E) (Fig. 1D) near the Cambodian border. The southern area comprised a sandy beach stretching from Bang Num Chet (13) (10°02′88.6″N, 99°10′94.3″E) (Fig. 1E) on the mainland to the Pitak Island, a small island of Chumporn Province, and Samui Island (14): Thongtanod Bay (9°24′56.7″N, 99°56′18.3″E) which belongs to Surat Thani Province. The Samui Island has two small connected islands, Kraten Island (9°23′06.80″N, 99°56′17.36″E) (15) and Mudsum Island (9°22′29.88″N, 99°58′37.00″E) (16) to the south, representing sites in the southern Gulf of Thailand (Fig. 1F). Each zone was characterized by habitat types present at sub-sampling sites (Table 1), and all zones are summarized in Table 2.
2.2 Sampling
The study was conducted during March to May of 2010–2015. Three transect lines were set perpendicular to the shore at each study site and extended from the Mean Low Water mark for approximately 30 m. Lines were separated by 20 m interval, and covered an area of approximately 1 800 m2. Percent cover along each transect was calculated following English et al. (1997). Dominant coral species, defined in terms of areal coverage, were recorded for coral habitats. Live and dead pinnids were counted and collected from 30 (1 m2) quadrats distributed equidistantly along each transect before calculated density. Water depth was also recorded for each quadrat, classifying burial depth as shallow (0–3 m), medium (3–6 m) or deep (>6 m).
2.3 Statistical analyses
Pinnid densities were compared among habitat types (coral reef, coral and rocky rubble, sandy sub-tidal bed, and sandy beach) and localities with one-way analysis of variance (ANOVA). Abundances were compared among plots to determine the manner in which the species were distributed across the submerged landscape. Morisita’s index (Iδ) of dispersion was used to illustrate spatial distribution, and chi-square (χ2) tests were applied to determine if the spatial distributions were random, uniform or clumped (Morisita, 1962). Water temperature, pH, salinity and conductivity were also measured three times at each quadrate using a YSI 556 MPS Handheld Multi-parameter instrument. All live and dead pinnid specimens collected were transferred to 70% alcohol.
Initial taxonomic identifications made in the field were tested by additional examination in the laboratory using monographic treatments of the Pinnidae, Turner and Rosewater (1958), Rosewater (1961), Swennen et al. (2001), Idris et al. (2008), and particularly the recent treatment by Schultz and Huber (2013). Basic shell morphometric data, including valve length and height, and byssus characters, were collected by using Vernier calipers (0.01 mm precision), and pinnid size was compared among the four habitat types. The physical character of the localities was compared by principle components analysis on the physical and chemical data. Pinnid compositions were compared among localities with non-metric multidimensional scaling (NMDS) analysis of inter-locality Bray-Curtis distances. The Bray-Curtis distance accounts for both similarity/dissimilarity of species composition, as well as the abundance of each species and also combined with sediment composition to analyse abundance factors. All analyses were conducted with the PRIMER software (Clarke and Warwick, 1994).
Burial depth (cm) was measured for each individual by measuring the distance from the buried umbonal region to the exposed posterior region of the valve. This transition area of shell is readily apparent on valves because of textural differences and the presence of epibiont organisms on the exposed posterior portion. Linear regression analysis was used to determine the relationship between shell length and burial depth, byssus thread characters among species.
Additionally, the exposed portions of valve surfaces or sediment water interface was compared among habitat types (coral reef, coral and rocky rubble, sandy sub-tidal bed, and sandy beach) of P. atropurpurea and A. vexillum with one-way analysis of variance (ANOVA). Independent t-tests were used to compare coral, and the mixed rock-coral habitats of P. deltodes.
3 Results
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3.1 Distribution
A total of 293 live and dead pinnid specimens were recorded at the sampled localities with P. atropurpurea being the most abundant (119 individuals), followed by A. vexillum (103 individuals) and P. deltodes (71 individuals). All three species (Fig. 2) were recorded in sediment of coral reefs and all mixed rock and coral sites (Figs 3a, b). Pinna deltodes lives on open sediment, grouped together between rock and coral rubble, with up to five individuals per group (Figs 3c, d). Pinna atropurpurea and A. vexillum occurred in sand beach and sand bed (Figs 4a–d), where both species are commonly buried in sand habitats and include sand substrate under coral, rock and coral (Figs 4a, b).
3.2 Abundance of pinnid species
All species are most abundant at shallow depths of less than 40 m, in water depth of 1–4 m and ranging 10–30 m from the shoreline (Figs 5 and 6). Pinna deltodes was most abundant at the Randokmai Island, where 18 individual were found (Fig. 5c). Pinna atropurpurea was most abundant at Mudsum (sand habitat, 66 individuals, Fig. 5f), whereas the abundance of A. vexillum did not differ among habitats, and was greatest at the coral reef at the Sai Bay (15 individuals, Fig. 6g).
Spatial distribution patterns of each species are shown in Table 3. All the species appeared to distribute uniformly at most sites (Morisita’s index, 0≤Iδ<1), although this could be influenced by low abundances at many sites. A zero index at the Yuon Cape, coral and rock rubble, Bang Num Chet, and sand beach, indicated that only one single individual was present in each experimental plot. Although the Randokmai Island, coral and rock rubble, and Mudsum Island, sand bed had I values indicating uniform distributions, those figures did not differ significantly from random (χ2=9.51 (χ2 0.95, df=6) and χ2=10.78 (χ20.95, df=3), respectively. No specimens occurred at the Praw Bay and Tharai Bay, and a single specimen occurred at the Kraten Island (Table 3).
Non-metric multidimensional scaling (MDS) similarities among the 36 sites clustered them into four groups (Fig. 7). Group 1 (G I) comprises coral reef sites of the Sak Island and Ngo Cape, from the Lan Island, Chonburi Province, where only one species, P. deltodes occurred, with 94.4% similarity among sites within the group. Group 2 (G II) comprise nine coral reef sites, including the east and west coasts of Changnoi and Sai Bay from Trat Province, where only A. vexillum was present, with 85.0% similarity among sites within the group. Group 3 (G III) is a large group consisting of 16 sites from mix coral and coral rubble habitats that show varied abundances of A. vexillum, P. atropurpurea and P. deltodes. Three main subsets were reported with 71.33% similarity within the group. Group 4 (G IV) comprises six sites, including two sand habitats where A. vexillum and P. atropurpurea co-occurred, but P. deltodes was absent in these sites (88.51% similarity within group). Abundances of pinnid dead shells found in each habitat were also compared (Table 4). Coral reefs showed the lowest percentage of dead shells, in contrast to sand beaches. Sand beaches contained large numbers of dead shells, including P. atropurpurea (36.36%) and A. vexillum (27.57%). Notably, A. vexillum consistently had the lowest numbers of dead shells. Pinna deltodes from rock and coral rubble habitats had greater numbers of death shells at (33.50%) compared to coral reefs (18.19%).
3.3 Density
Densities of the dead and live pinnid based on locality varied from not zero (absent) (open coastline at the Tharai Bay and Praw Bay, with strong wave action), to a maximum 2.67 ind./m2 at the Mudsum Island, where the locality is a sheltered coastline with sand beds (Table 5).
The most common pinnid species, A. vexillum, had its highest density at the Sai Bay, coral reef ((0.50±0.16) ind./m2), but that did not differ significantly from other sites (F=2.391, p=0.07, df=464). Pinna atropurpurea had its highest density ((2.20±0.36) ind./m2) at the Mudsum Island, a sand bed habitat, and this density was significantly greater than those at other localities (F=17.634, p=0.009, df=464). Pinna deltodes was recorded only from coral and rock rubble and coral reef habitats, and the three localities of greatest densities were from coral and rock rubble of the Sichang Island, Chonburi Province, and the inner Gulf of Thailand. The Randokmai Island ((0.60±0.15) ind./m2), Hintasin ((0.57±0.22) ind./m2) and Ngo Cape ((0.43±0.16) ind./m2) differed significantly because of low densities. These are coral habitats from Trat Province, and the latter two from Surat Thani Province (F=3.486, p=0.01, df=377).
Atrina vexillum was significantly most abundant at coral reef habitats ((1.90±0.56) ind./m2 (F=4.446, p=0.005, df=116)), whereas P. atropurpurea was most dense at sand habitats, including sandy beaches ((0.37±0.01) ind./m2) and particularly sand beds ((2.90±0.48) ind./m2) (F=13.961, p=0.009, df=116). Pinna deltodes was most dense at rock and coral habitats ((1.60±0.42) ind./m2), and was greatest at coral habitats ((0.77±0.17) ind./m2), although this did not differ significantly between the two sites (t=1.89, p=0.07, df=58) (Fig. 8).
3.4 Shell size frequency, shell burial and byssus thread characteristic
Shell length of P. deltodes did not differ significantly among habitat types (t=2.98, p=0.10) (Fig. 9). However, individuals from coral reefs and mixed coral and rock of species P. atropurpurea (Fig. 10) and A. vexillum (Fig. 11) were significantly larger than those from sand beaches (F=5.50, p=0.002 and F=18.53, p=0.001, respectively).
Maximum sizes of those species in coral reefs and mixed coral and rock habitats ranged from 36 to 40 cm, but those in sandy habitats ranged from 21 to 25 cm, with averages of (22.11±1.15) cm (mean±SE) for P. atropurpurea (Fig. 10) and (15.61±0.77) cm for A. vexillum (Fig. 11).
In terms of byssus thread characteristics, P. deltodes had significantly fewer threads (13.95±4.36, F=3.74, p=0.03) and were significantly shorter ((5.34 ±0.74) cm, F=5.98, p=0.003) than other species, although the diameter of the byssus mass and the burial depth was not significantly different among members of the family. Whereas A. vexillum showed significant difference in mass of byssus thread, measured by diameter bundle ((0.58±0.02) cm, F=0.27, p=0.04) (Table 6). The correlations between shell length and boring length of all pinnids showed the same trends of positive correlation by linear regression and coefficient of determination (r2). Significant correlations were found in A. vexillum and P. atropurpurea. The strongest correlation was between shell length and boring length in A. vexillum (r2=0.79, p=0.000 1) and linear equation; y=0.770 4x+0.719 8 (Fig. 12b). This was followed by P. atropurpurea (r2=0.34, p=0.001) with linear equation; y=0.304x+6.857 (Fig. 12a). The linear regression of shell length and boring length in P. deltodes was not significant (r2=0.27, p=0.06) with linear equation; y=0.438 0x+2.785 3 (Fig. 12c). In terms of correlations between shell length and characteristics of byssus threads, the shell length of A. vexillum was positively correlated with byssus thread length and the number of byssus threads by linear equation; y=0.412 9x–0.084 0 (Fig. 12e) and y=19.371 5x–235.341 (Fig. 12h). However, only byssus thread length was significantly correlated with shell length (r2=0.24, p=0.000 3). Shell length of the genus Pinna was not significantly correlated to any byssus thread characteristics.
Exposed valve portions were compared among habitat types. Populations of P. atropurpurea and A. vexillum from sand beaches showed significantly shorter distances from the sediment-water interface than species in other habitat types. The shortest open shell area for epibiont attachment was (1.288±0.219) cm for A. vexillum (F=5.83, p=0.002, df=49) and (2.38±1.64) cm for P. atropurpurea (F=41.08, p=0.000 1, df=73) (Fig. 13).
3.5 Environmental parameters
Seawater temperature ranged 30.30–35.23°C, with maximum temperatures at three coral sites: Trat Province, western and eastern coast of Changnoi and Sabbarot Bay of Chang Island (Table 5). Water pH was alkaline, ranging 7.80–8.63, conductivity ranged from 47.87 to 66.93 ms/cm and salinity varied between nearly normal and high, 30.99–36.49. (Table 7). Maximum salinity and conductivity were recorded in the south of Thailand, the Thongtanod Bay having the highest salinity (36.49±1.33) and Mudsum having the highest conductivity ((66.93±0.04) ms/cm). The Sabbarot Bay had the highest levels of suspended solids, (36.18±16.75) mg/L whereas the lowest was recorded at the Thongtanod Bay, (16.55±1.71) mg/L (Table 7).
When each sampling site was linked to five environmental variables that showed low coefficient correlation as Fig. 14, the maximum was 0.500 at salinity and suspended solid (Fig. 14). High abundance of P. atropurpurea was correlated to sites with high percentage of sand composition in sediment. In sand habitats, sand bed and sand beach showed higher than 60% of sand composition (d symbol categories) found high P. atropurpurea abundance (large area of bubble circles) (Fig. 15A). However, percentage of sand sediment could not explain any pattern in A. vexillum abundance because high abundance of A. vexillum (large area of bubble circles) was found in all range of sediment composition (a to d symbol categories) (Fig. 15B). High abundance of P. deltodes was mainly found at 10%–29% sand composition (b symbol categories) (Fig. 15C).
Because P. deltodes was specifically found in coral reef and coral and rock rubble habitats, several factors such as rock composition and coral type were used to find correlated pattern. Most likely P. deltodes abundance increased (increasing size of bubble circle) when sites had more than 20% of rock composition (c to d symbols categories). Whereas P. deltodes prefer any sites that composed of 20%–60% dead coral and 10%–30% lived coral (Fig. 16). Where the percentages of rock, dead coral or lived coral were similar to sand composition could not be used to explain the abundance of A. vexillum (Fig. 17).
4 Discussion and conclusions
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Atrina vexillum, a species with a very broad shell, is an Atrina species that has a broad distribution (from the Red Sea to the Philippines, including the Gulf of Thailand) (Schultz and Huber, 2013; Silina, 2012). Although A. pectinata and A. chinensis were report on the coast of western Thailand in the recent review on Pinnidae (Schultz and Huber, 2013), it was absent in this study because the habitats surveyed did not include muddy sand. The species diversity found in the Gulf of Thailand was lower than that reported in Sungai Pulai, South Western Johor coast, Malaysia (seven species) where higher diversity was recorded in seagrass habitats, with species consisted of P. muricata, P. bicolor, P. incurve, P. deltodes, P. atropurpurea, A. pectinata and A. vexillum (Idris et al., 2008). Many large pinnid species around the world are found in islands and some pinnid species occur between the islands in the gulf. These species include P. carnea, which usually occurs between the islands of Bermuda (Yonge, 1953), and P. nobilis which is commonly found on islands within the Mediterranean, such as Antioco Island in the Gulf of Oristano (Addis et al., 2009), Djerba Islands in the Gulf of Gabes (Rabaoui et al., 2010), Columbretes Island (García-March and Márquez-Aliaga, 2007) and areas around the island of Majorca and the Balearic Islands in Spain (Hendriks et al., 2013). The islands in the Gulf of Thailand were one of important habitats for pinnid populations which mostly occur close to islands. The Gulf of Thailand is a semi-enclosed extension of the South China Sea. The current systems in the gulf include a surface current pattern during the northeast monsoon that moves from the South China Sea, past China and down to the Gulf of Thailand from December to May (Chansang et al., 1999; Yanagi et al., 2001). There is also a southwest monsoon that moves along the Sunda Shelf, from Peninsular Malaysia up to the Gulf of Thailand from June to November (Chansang et al., 1999; Yanagi et al., 2001). Then islands in the Gulf of Thailand are sheltered habitats with a high abundance of pinnid species. However, two sites in the Gulf of Thailand (Tharai Bay and Praw Bay) were with abundance of no pinnid species in spite of the presence of ideal habitat characteristics, such as an open coastline facing strong sea waves. This finding was similar to that of Rabaoui et al. (2008) who also found no pinnids in expected sites on the Tunisian coast. They proposed that the absence may have been due to recent habitat modifications due to environmental conditions.
Pinnidae were found at varying depths in the sub-tidal or intertidal zone (Butler and Brewster, 1979; Butler and Keough, 1981; Butler, 1987; Katsanevakis, 2006; Rabaoui et al., 2008, 2010). Shallow intertidal water depth (no more than 4 m) was preferred by pinnid species in this study. This study demonstrated that the Gulf of Thailand provides details on microhabitats and the distribution of pinnids at a species level. Interestingly, pinnids were found in sites with four different habitats, including sand beaches, sand bed coral reefs and coral mixed with rock. This could explain the distribution flexibility of this family which occur over a broad habitat range. The finding could support Katsanevakis (2006) who asserted that habitats for Pinna are not specific; they do not require only seagrass meadows, and they can exist in bare soft sediment as well.
A clumped distribution pattern has been found in pinnids from many places around the world. These species include P. nobilis (Coppa et al., 2010; García-March et al., 2007a) and P. rudis (Nebot-Colomer et al., 2016) from the Mediterranean Sea, and P. bicolor from South Australia and South Western Australia (Butler and Keough, 1981; Butler, 1987). Pinnid individuals tend to be attracted to particular locations within an environment. Aggregation patterns in pinnids may be explained by higher survival in particular habitats (Begon et al., 1996).
The distribution of the three pinnid species this study surveyed were uniform in distribution following the Morisita’s index, meaning that pinnid populations presented with one or more individuals per plot. A maximum of five individuals were found per plot, although some sites had none or only one individual per plot. Generally, a regular or uniform dispersion is a common pattern in forests and monoculture plantations where there is competition between individuals or positive antagonism that promotes uniform spacing in land reference (Odum, 2004). This uniform pattern was demonstrated in most coral reef habitats, which demonstrates a successful adaptation to competition in limited sediment space for pinnid larvae. Other sites, such as Mudsum which had sand beds and reefs and the Randokmai Island which had coral and rock rubble, presented uniform patterns that were not significantly different from a random distribution. These habitats provided a homogenous space or stable area as sediment for larvae to settle. This may support the random distribution of pinnid species occurring in the open and in huge gaps of sediment. This case was similar to studies of P. nobilis which found that random distribution occurred in sea beds dominated by meadows of seagrass in the Moraira Bay (García-March et al., 2007b) and Lake Vouliagmeni (Katsanevakis, 2006). Katsanevakis (2006) suggested that dispersion of pinnids was related to quadrate size. Random distribution of pinnids occurred in small quadrats in small-scale samples whereas aggregated distribution was found in large-scale samples. The positive correlation of dispersion indices with quadrat area may be related to the corresponding scale of patchiness in an environment. Our study could attribute the flexible distribution of pinnid populations to differences in sediment space and habitats required by larvae. Then clumping in pinnids is not gregarious behaviour because in some habitats, a random distribution pattern was shown, indicating possible ecological reasons behind population distribution.
Pinnidae abundance in sand habitats, such as sand beds and sand beaches, were significantly different from pinnids in coral habitats. It is possible that sand habitats provided particularly substrate for supporting the abundance of A. vexillum and P. atropurpurea that different from coral. Yonge (1953) described the habits that Pinnidae always live embedded vertically in soft substrata with enough underlying gravel to provide byssus threads attachment.
Density of pinnids in the Gulf of Thailand varied from site to site, with some sites containing no individuals and others containing 2.67 ind./m2 (maximum density found). Although, the Gulf of Thailand is geographically small, the high density values found in this area are indicative of healthy populations. The figures found in this study are much higher than other species in the Pinnidae family in regions that developed during a similar time frame (approximately 2000 BC) (Šiletić and Peharda, 2003; Katsanevakis, 2006; Idris et al., 2008; Rabaoui et al., 2008; Caronni and Navone, 2010; Fryganiotis et al., 2013; Hendriks et al., 2013). The density of Mediterranean Pinna, such as P. nobilis, ranged from 0.002 to 0.20 ind./m2 in seagrass and rocky substrate (Šiletić and Peharda, 2003; Katsanevakis, 2006; Rabaoui et al., 2008; Caronni and Navone, 2010; Fryganiotis et al., 2013; Hendriks et al., 2013). Another Mediterranean species, P. rudis, ranged from 0.0 to 6.89 individuals per 100 m2 (Nebot-Colomer et al., 2016). Thai pinnids, mainly from corals and sands habitats, showed higher density than pinnids in the seagrass habitat of Sungai Pulai, South Western Johor coast of Malaysia in the South China Sea region (less than 0.02 ind./m2) and the seven pinnid species reported by Idris et al. (2008). The difference in density can be explained by larvae survival and accumulation differences. Nebot-Colomer et al. (2016) suggested that areas with the highest densities commonly indicate an optimum area for larval growth and settlement.
Pinnidae are suspension-feeding bivalves that often depend on the local productivity of phytoplankton as a food source (Newell, 2004). Among many environmental factors, the growth and survival of Pinna juveniles is influenced by the presence of chlorophyll a and particle organic matter (Acarli et al., 2011; Silina, 2012). Many researchers suggest that food availability is an important factor influencing the density in Pinnidae populations (Wu and Shin, 1998; Šiletić and Peharda, 2003; Silina, 2012). The Gulf of Thailand receives discharges from four main rivers (in the northern part of the gulf) which contribute important sources of nutrients for phytoplankton photosynthesis (Buranapratheprat et al., 2008). In this area, Chalermwat and Lutz (1989) reported extensive aquaculture, especially for shellfish. Shellfish, including green mussel, oyster and blood clam, are intensely farmed in this area. In addition to food availability, warm water temperatures (particularly warm bottom temperatures throughout the year, i.e., 30–35°C in the Gulf of Thailand; Yeemin, unpublished data) may also help the settlement of pinnid larvae. Growth of newly settled young pinnid is rapid in shallow waters and in the summer months (Butler and Brewster, 1979; Richardson et al., 1999; Katsanevakis 2006; Silina, 2012). Highly productive and suitable environments contribute to the density of pinnids in Thai coastal areas and may be selected by pinnids as habitats in the future.
Effective wave sheltering was an important factor in explaining the high density of pinnids in small-scale populations. Mostly pinnid populations that were assessed tended to be denser in sheltered locations than in more exposed ones (García-March et al., 2007a). For example, P. nobilis appear in denser populations when they are sheltered from the hydrodynamic forces of wave action (Hendriks et al., 2011). The same trend is seen in populations of P. rudis, which use caves as sheltered habitats and are highly concentrated in these areas compared to low densities in other habitats (e.g., rock, sand and seagrass) (Nebot-Colomer et al., 2016). High densities of P. nobilis found in Mediterranean waters indicated that this species may favour settlement of larvae at low wave period and intensity in heterogeneous sediment (Richardson et al., 1999; Katsanevakis, 2006; Rabaoui et al., 2008).
The highest densities of pinnids in the Gulf of Thailand occurred in sand beds, back reef, and the enclosed coastlines of coral reefs or small islands. These habitats using coral reef as barrier to face strong sea wave and large area of sand beds behind reef provide suitable substrate for fan mussel larvae settlement. It might be concluded that pinnid population use indirect benefit of the coral reef to form a community. However, no information has been reported about the relationship between water speed and coral size (García-March et al., 2007b). The large sand beds in this study are similar to habitat characters reported for P. bicolor from the Gulf St. Vincent off the coast of Edithburgh, South Australia. These P. bicolor populations had a maximum density of 2.8–2.6 ind./m2.
The low pinnid density found in sand beaches may be related to the high mortality rates found in this study. This habitat had the highest number of dead pinnid shells any other habitats. The cause of mortality in sand beach habitats can be explained by their shallow depths; it is particularly difficult to live in very shallow waters (less than 1 m of water depth) in this area. Some uprooted dead shells and injured shells might be the consequences of hydrodynamic stress from seawater and predators attracted at low tide. Many researches demonstrated the depth and predators as the main factors for pinna mortality. The correlation of depth with environmental factors can be explained by habitat distribution and food productivity (Katsanevakis, 2006, 2007). A significant correlation between fan shell density and depth was demonstrated by Rabaoui et al. (2010). They found no presence of P. nobilis in waters shallower than 0.3 m; below this depth, density increased with depth. Moreover, García-March et al. (2007a, b) showed that hydrodynamic stress was reduced in deeper areas, and it controlled the density of P. nobilis in the Moraria Bay in the western Mediterranean.
Another possible reason for shell death in sandy beach habitats is the increase in predation pressure (Šiletić and Peharda, 2003). Benthic predators observed in our study were mainly the long-spine sea urchin (Diadema setosum) and crabs. These were found in high numbers in the study sites attached to the posterior shell. This was similar to a report of the mortality from transplanted P. bicolor predominantly caused by crabs and fish (Wu and Shin, 1998). Shell damage by predators can expose soft tissues and increase sensitivity to other causes of death (Dietl and Alexander, 2005). Mortality in shallow waters can also be caused by the harvesting of larger individuals by humans (Katsanevakis, 2006, 2007; Rabaoui et al., 2008). The high visibility of these shells may partly explain the low density in this habitat compared to others in the Gulf of Thailand.
The shell morphology and behaviour of Pinnidae species could be the cause of differences in mortality. The lower mortality of Atrina species than Pinna species from all habitats in this study may be explained by the natural round shape and the shorter hinge line with a broad byssal sinus (Yonge, 1953; Stanley, 1970; Schultz and Huber, 2013). In terms of behaviour, Atrina species bury themselves more completely and deeply in the sediment than Pinna species (Yonge, 1953; Richardson et al., 1999; García-March et al., 2007a). This not only decreases the opportunity of predator contact but also reduces the chance of being washed out to sea by waves and desiccated during low tide (Neubauer et al., 2013). Stanley (1970) found that A. rigida buried themselves more deeply than P. carnea. Stanley (1970) also found that A. rigida was more effective at anchoring themselves in the sediment and had a deeper burrowing mechanism, since its periodic muscular contraction was apparent during ontogeny.
The general size of pinnid specimens in the Gulf of Thailand ranged from 11 to 40 cm. The genus Pinna was similar in size to P. bicolor from Australia (Butler and Brewster, 1979). Butler and Brewster (1979) reported size-class by the modal length and estimated the age of P. bicolor by size: year-old shells should be 20 cm, two-year-old shells should be 26 cm and three-year-old shells should be 35 cm or longer. It is common for this family to show variable success in recruitment and a growth rate which decreases with age (Butler and Brewster, 1979; Idris et al., 2008; Silina, 2012).
Size frequency distribution of the three pinnid populations in our study among the four habitats showed that the largest shell lengths were from coral or coral associated areas such as coral and rock rubble and sand bed back reef. The sand beach habitat had a high frequency of the smallest shell size (11–25 cm). There are two main reasons why different shell sizes would be found in different habitats. First, shell size in the family Pinnidae may be related to the growth curve of the animal or the physical factors in the study site (Richardson, 1999; Šiletić and Peharda, 2003; Rabaoui et al., 2008; Idris et al., 2011; Silina, 2012). Second, larger size of the same species may result from older individuals staying longer under fewer disturbances. García-March et al. (2007a) showed that large individuals of P. nobilis survived by being completely hidden by the leaves of Posidonia oceanica in Mediterranean water. While pinnids from sand beaches may have a higher frequency of younger shells than other habitats, small shell size may also be selected by the mortality pressure as previous discussion. For example, Katsanevakis (2007) and García-March et al. (2007a) demonstrated that natural mortality was strikingly size-dependent in P. nobilis, suggesting that the likelihood of mortality increased as fan mussels grew in size. Rabaoui et al. (2008) suggested that the high frequency of small P. nobilis individuals in sandy and shallow sites on the Tunisian coast may be because the site is a recruitment area for juveniles. In this study, small shell size may improve survival rates in sand beaches at low tide. This case was similar to the study on transplanted P. bicolor, Wu and Shin (1998) demonstrated that young and small individuals were protected from high flow speeds. Another possible advantage of small shell size is the short distance in the sediment-water interface on posterior side which may protect from predation or prevent the shell mantle being exposed to air. It was demonstrated in both Atrina and Pinna at the sand beaches site. Pinnidae has the capacity to withdraw the mantle and squeeze the shell edges together. Mantle retraction and flexible margins are advantageous in surviving marginal injuries (Yonge, 1953) and speeding up the regeneration of damaged shells (Dietl and Alexander, 2005).
Members of Pinnidae always live vertically embedded in soft substrata, using byssus threads to attach themselves to gravel (Rosewater, 1961; Yonge, 1953) and in crevices or cement themselves to substratum (Schultz and Huber, 2013). Survival of byssates living in each habitat probably depends on adjustments of their thread character or the development of boring mechanisms (Printrakoon and Tëmkin, 2008; Pearce and La Barbera, 2009).
This study demonstrated that members of Pinnidae increase their boring depth when shell length increases to prevent dislodgment from sediment in the same trend of all pinnids in all habitat types. However, Atrina shows more effective byssus threads in the burrowing mechanism by increase length and number of byssus threads when shell size increases. This makes Atrina a stronger, deeper borer than Pinna which may also make it less susceptible to mortality.
Composition of sediment characteristics was an important factor in determining the species type and abundance of Pinnidae in this study. Our results concurred with those of Addis et al. (2009) who suggested that settlement and distribution of Pinna in estuarine and unvegetated sea floors would be determined by sediment. Pinna have been reported as living primarily in sandy sediment (Stanley, 1970). Populations of P. atropurpurea in subtidal areas use byssus threads to attach themselves to soft muddy sand in the Indo-Pacific region (Schultz and Huber, 2013). A high abundance of P. atropurpurea occurred in habitats with very high soft sediment composition (more than 60%), particular sand habitats (sand beds and sand beaches), throughout the Gulf of Thailand. Pinna individuals need more sand since it is the appropriate substrate for the settlement and survival of larvae. Since Pinna shell is very large, elongated and thin, it can only be buried in the sediment to about half the shell’s length (Stanley, 1970).Therefore, sandy sediment may enhance a stable vertical position without uprooting the shell.
Generally, P. deltodes prefers hard substratum of either rock-strewn reefs of coral blocks and head (Scheltema, 1983; Schultz and Hubber, 2013). Moreover, Schultz and Hubber (2013) reported that P. deltodes individuals shallowly buried themselves in sand among these hard substrates, coral and rock reef. Idris et al. (2008) reported that rocky shore areas from the south part of Peninsular Malaysia were the habitat for P. deltodes.
Rock and coral habitats of the Gulf of Thailand are an appropriate habitat for this species which prefer sites with more than 20% rock composition. This study revealed that P. deltodes used the shortest byssus threads and the lowest number of byssus threads for sediment attachment than any member of Pinnidae. Some of P. deltodes live behind rock or orientate themselves at narrow angles to bottom instead of boring deeper into sand sediment. Interestingly, Schultz and Huber (2013) reported finding some specimens oriented horizontally under coral blocks. The byssus of this species allows attachment to a variety of surrounding broken rocks or coral fragments (Printrakoon, pers. obs.). Similar to P. nobilis, one of the largest mollusc species, typically occurs in association with Posidonia oceanic meadows. This fan mussel utilizes the rhizomes and shoots of P. oceanic to attach their numerous byssus filaments to anchor themselves and live partially buried upright in the sand (Coppa et al., 2010; Hendriks et al., 2011).
In this study, A. vexillum was found buried in various sand sediment compositions. Its shell is round with a short posterior end, which is advantageous for burial in small spaces or shallow sediment (Yonge, 1953; Schultz and Huber, 2013) of various habitats including sand, coral sand and sandy mud in seagrass flats. Its versatile shape explains why A. vexillum was commonly found in all sites and also the highest density was specifically found in small limited sediment gap under coral reef habitat.
In summary, the Gulf of Thailand is an important place for Pinnidae populations, and it provides varied habitats that benefits high density and biomass. Coral reefs are one of the most important marine habitats in shallow tropical seas, and they provide a number of important ecosystem services (Moberg and Folke, 1999). Coral reefs are mainly found fringing islands in the Gulf of Thailand. This habitat and the seagrass provide direct and indirect shelter for Pinnidae. In terms of production, reefs provide structure and act as focal points for secondary producers. Also, shelter from hydrodynamic forces in reefs enhanced by increasing sedimentary fluxes may increase food supplies to support large filter-feeder bivalves (Moberg and Folke, 1999). However, habitat destruction and over-exploitation of pinnids as a food source may be an important factor limiting pinnid population density in the future. The database constructed during the course of this study will assist in understanding the ecology of the family Pinnidae and will inform management and conservation efforts in the future.
Acknowledgements
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The authors thank Lakeside Fund, California Academy of Sciences for support and fund to confirm shell specimens, and Marine Biodiversity Research Group, Ramkhamhaeng University, for assistance in survey and scuba diving for collecting specimen.
Funding
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  • The Thai Research Fund, Office of the Higher Education Commission, KURDI and PRF from Faculty of Science, Kasetsart University.
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doi: 10.1007/s13131-018-1230-4
  • Receive Date：2017-07-27
  • Online Date：2026-03-31
  • Published：2019-02-25
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  • Received：2017-07-27
  • Accepted：2018-02-01
Funding
The Thai Research Fund, Office of the Higher Education Commission, KURDI and PRF from Faculty of Science, Kasetsart University.
Affiliations
    1 Animal Systematic Special Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
    2 Department of Invertebrate Zoology and Geology, California Academy of Sciences, San Francisco, California 94118, USA
    3 Department of Biology, Faculty of Science, Ramkhamhaeng University, Bangkok 10240, Thailand

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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