Existence, Growth and Reproduction of Pearl Oyster Pinctada Margaritifera in Hadhramout Coast/Gulf of Aden

Egyptian Journal of Aquatic Research (2014) 40, 473–481

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FULL LENGTH ARTICLE Existence, growth and reproduction of pearl oyster Pinctada margaritifera in Hadhramout coast/Gulf of Aden

Moteah Shaikh Aideed, Basmidi Abdulla Ahmed, Ali Attaala Mukhaysin *

Department of Marine Biology, Faculty of Environmental Sciences and Marine Biology, Hadhramout University, Mukalla, Yemen

Received 3 October 2014; revised 11 December 2014; accepted 19 December 2014 Available online 6 January 2015

KEYWORDS Abstract This study was conducted to conﬁrm the existence, morphological and biological attri- Pinctada margaritifera, butes; growth indicators and reproduction of pearl oyster, Pinctada margaritifera in Hadhramout Growth; coast. The samples were collected from around coral colony bases from the shore bays of the city Reproduction; of Mukalla, Broom and Bir Ali Islands through the period September 2009–November 2010. 213 Hadhramout coast specimens were collected from shallow habitat at intertidal zone, subtidal up to more than 15 m in some places. Its morphological characteristics were described. The results show a strong positive correlation (R2 = 0.9836) between the biometric parameters (ShH and ShL) of P. margaritifera, with an equation of: Shell Length = 0.992 · Shell height0.995. The maximum size of the recorded species was180 mm. Growth rates retreated with age from an average of 34.6 mm/2nd year to 3.7 mm/the 7th year. The dominant proportion of ripe mature specimens was recorded in December 2009–March 2010 in females and along two periods in males – January–March and August– October 2010. The data showed that mean gonadic index (GI) transition of males and females followed nearly the same pattern. The results revealed that the occurrence of both adults and juveniles individuals indicates that the Hadhramout coastal environment is suitable for the growth and reproduction of pearl oyster. ª 2014 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction of feeding physiology, reproduction, breeding, farming and bio-environmental relations for this animal in different regions The success of pearl oysters farming in the South Pacific and of its distribution. Indo-pacific Islands in twentieth century leads to increased The pearl oyster was considered one of the marine organ- interest and research in its environments and biology in most isms that was cared by Arab man since prehistoric era, being countries of tropical seas. The research focused on the study the most important, if not the only source of precious pearls. It was certainly prevalent in the Arabian Gulf as a marine animal, separated and designated species, with its own biological * Corresponding author. E-mail address: [email protected] (A. Attaala Mukhaysin). behavior there, even before Laine´s natural Encyclopedia takes Peer review under responsibility of National Institute of Oceanography its scientific position (Linnaeus, 1758; Strack, 2006, 2008). It is and Fisheries. found in many parts of the seas and bays of the Indian Ocean, http://dx.doi.org/10.1016/j.ejar.2014.12.004 1687-4285 ª 2014 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 474 M.S. Aideed et al. in particular in the Gulf or the Strait of Mannar and the Bay of attributes; growth indicators and reproduction in Hadhramout Bengal (Hylleberg and Kilburn, 2002). Naturally it is coast. It is the first report that looks in the pearl oysters’ widespread in the Western and Central Pacific, including the community in Hadhramout coast and the Gulf of Aden at all. Hawaiian Islands. Pearl oyster cultured in pearl production farms in the Materials and methods islands of French Polynesia, the Cook, the Marshall and Salmon Islands; in southern China, northern and Western Study area Australia; in Seychelles and Sudan (Pouvreau et al., 2000a). Attention increased recently in most parts of the distribution of all Pinctada spp.; they were given a great concern by The study was directed to start to focus on the samples scientists for its environmental and economic considerations, collected from around coral colony bases and in the shore bays and being the best sources of the global jewelry trade. of the city of Mukalla (1430N 4910E), area of Broom Detailed studies on the growth and reproduction of these (1420N 4859E) and Bir Ali Islands (1359N 4827E) within species have been done in all their distribution areas, from the coast of Hadhramout (Fig. 1) through the period Australia, Japan and Korea (Colgan and Ponder 2002; Yoo September 2009–Novrmber 2010. The sample constitutes 213 et al., 1986; Numaguchi and Tanaka, 1986); via Arabian Gulf specimens at all. These sites are characterized by relative (Mohammad 1976; Al-matar et al., 1993b); up to Mexico shallowness, which ranged between 3 in Broom and 12 m in (Lodeiros et al., 2002); how is paradoxical, except in Gulf of Mukalla. In these sites a little plant cradle, dominated by Aden. coherent rocky bottoms that are interstitial with a sandy Despite the fact that very little is mentioned about the role bottom with some coral formations, was subjected periodically of the Gulf of Aden in the history of pearl oysters’ fishery and to currents of annual upwelling escalating during the summer harvest, the city of Mukalla was pointed out as one of Arab months – June to September. ports that handled trade of pearls until the beginning of the Some samples showed that it was packed with dead and live twentieth century. It could be considered as a place of gather- organic growths (Fig. 2), thus we scraped off attached foulers ing from the adjacent coasts, in particular of the kind what was and the shells were cleaned. Linear morphological measure- then called (Sadaf), a current type of Pinctada margaritifera. ments were recorded (Fig. 2) to the nearest mm using Digital There is also anecdotal evidence, that suggests that some Stainless Steel Vernier Caliper (Mitutoyo). Initial measure- Sudanese with the help of the British people might have ments included the shell height or the length of the distance worked in the purchase and reaping of the oyster shells and between the joint at the front top of the shell and the outer exported to unknown destinations. In addition to that, they shell end (ShH) or the inner edge of the limits of the nonnacre- worked on containing the living oysters in submersible frames ous border excluding the digitate growth processes (dorsoven- (perhaps its culture) in a place near the present port southern tral measurement (DVM); length of the shell (ShL) which to the city of Mukalla up to the end of the fifties of the last shows the widest distance in the center of the shell; and the century (interview old fishers). What increases the belief in length of the joint (HL) (Fig. 2). The total weight of the animal the veracity of oyster gathering and culturing is the experiment (T Wt) was recorded, the weight of the animal without shell of cultivation and planting of pearls in Sudan on the Red Sea (body weight – B Wt), weight of the empty shell (Sh Wt), (Khor Dungunab and Peninsula Rouet), in the first quarter of and the weight of the separated gonads (G Wt), to the nearest the last century. Those experiments might be needed for mother of pearl from shells of that type which existed in 0.1 g using a digital balance. Hadhramout coast. For studying the variation in relationship between some Pearl oyster – P. margaritifera was recorded as a species shell dimensions during various growth stages, the data were over the last three centuries although it is awarded many scien- grouped into length classes with a class interval of 20 mm. tific names (Reeve, 1857; Iredale, 1915; Hynd, 1955; Ranson, The length–weight relationship was calculated using the Excel 1961; Rao, 1968; Blanc and Durand,1989; Arnaud et al., software. 2002; Hwang and Okutani, 2003; Masaoka and Kobayashi, Growth studies were done by calculating and measuring the 2006); but it remains overshadowed for exploitation and growth rings in the shells following Richardson (2001) and scientific researches in the Gulf of Aden, in particular in the Coakley (2004). southern coast of Yemen despite many collection and exploita- For sounding physiological changes of sexual development tion in the antique industry, pearl cultivation and production of this animal, we draw these changes through visual and in the neighboring seas and gulfs as the Red sea, the Gulf of microscopic inspection of smears from the fresh sexual glands Oman and the Arabian Gulf (Elnaiem, 1984; Nasr, 1984; of females and males, that was followed by many researchers Mohammed and Yassien, 2003; Al-Khayat and Al-Ansi, (Lucas and Beninger, 1985; Guillou et al., 1990; Pouvreau, 2008). 1999; Kimani and Mavuti, 2002; Kimani et al., 2006; Le In recent years, attention has risen and directed toward an Moullac et al., 2012), which gave us a dependable result in increased environmental and economic impacts on communi- the preliminary determination and reading of the nature of ties of coastal marine organisms due to the effectiveness of sexual reproductive cycle of this important mollusk for the first overfishing by the commercial and artisanal fishing boats time in Hadhramout coast environment. which prevailed for some time and continues today along the After studying samples and reviewing the references in the southern coast of Yemen, making this region touted as reproduction of Pinctada genus we partially adopted a gradual emptied of its basic living wealth. criteria proposed by Pouvreau et al. (2000a) and Pouvreau Thus, the present study aimed to confirm the existence of et al. (2000b) for P. margaritifera to 6 stages of maturity for the pearl oyster and identify the morphological and biological the reproductive system: Existence, growth and reproduction of pearl oyster Pinctada margaritifera 475

Fig. 1 Study sites where samples were collected.

Fig. 2 Exterior view and oysters shells’ morphological measurements and the difference between covered by fouling (a) and free shells (b). 476 M.S. Aideed et al.

Stage 1: indeterminate or inactive, no signs of sexual activ- Previous studies review efforts which failed to find any ity, the sex marked by ‘‘J’’. documentary indication on the record of black lip pearl oyster Stage 2: early development, mature gametes are not in the Hadhramout coast; until today registration of this observed, the sex marked by ‘‘II’’. animal is not documented officially even in the Gulf of Aden. Stage 3: late active development, near ripe follicles with vis- Consequently, the current study has the right to register its ible small mature gametes, the sex marked by ‘‘III’’. presence and distribution in the Hadhramout coast and the Stage 4: spawning ripe, follicles distended, confluent and Gulf of Aden for the first time. entirely filled, the sex marked by ‘‘IV’’. Stage 5: ripe stage, maturation, partially spawned, the sex Morphology and structure marked by ‘‘V’’. Stage 6: fully spawned, spent, with empty and thin gonads, It was found that the morphological characteristics for this with reabsorbing and few residue mature cells, the species in the coast of Hadhramout were a half circular shell sex marked by ‘‘VI’’. form and discoloration of mother of pearl edge of the inside shell. The latter colored in silver with gradation toward outer The quantitative indicator of the reproductive state we frame painted smoky dark with something of iridescence red adopt the most widely used gonad index GI. This index is use- and green on the borders of mother of pearl area, turns to ful to determine potential spawning period. In our study, GI strong darkness for the mother-of-pearl-free region. Another was computed for each individual, by using the following characteristic is the ampleness of the shell size expressed by equation: height, as much over every other species and up to 18 cm,

GI ¼ WGonad=WShell width and length of the joint or the anterior pole, as characterized by the absence of completely articular teeth (Fig. 3). where WGonad is the wet tissue weight of (gonad + digestive At a time where there is mixing and confusion in the classi- gland) and WShell is the weight of shell (in g). fication of many species of this genus (about 11 species accord- Given the irregular sampling and few in number, and the ing to Ranson (1961)), and in particular those that prevail in fact of the absence of one sex in certain months, we prefer to the waters between Australia, China and Japan (East Asian – integrate the males and females to draw preliminary important Pacific to the Hawaiian Islands), the species P. margaritifera, indicators that allow understanding and determining bio- widespread in the Western Pacific, Indian ocean, and is found ecological situation of the animal in this region. in the coast of Hadhramout could not be suspected (Figs. 2 and 3), and easily diagnosed and recognized from all the Results and discussion remaining species, even the closest one – P. maxima. The latter, although similar in size and with the absence of articular teeth, Habitat and distribution the spreading circumference did not reach to the Gulf of Aden yet (Bartsch, 1931; Yu and Chu, 2006). It has been pointed since the beginning of the study of this According to the filed underwater observation we found that species (Tranter, 1958) to the extent of variability in the shape, the species P. margaritifera in Hadhramout coast usually inha- biological and an environmental characteristics of black lip bit under big stones and rocks, in crevices and corners of the pearl oyster, P. margaritifera according to different parts of hard bottoms, rarely observed among aggregation of algae, its presence that wide-ranged from Australia to Panama and dispersed in a limited range among the coral habitats, and if from the Red Sea toward the Persian Gulf and the Gulf of any, it attached to the corners of the brain corals species of Leptoria phrygia and Platygyra daedalea; sometimes we found it under the species of Pavona maldivensis and near massive coral of Porites lutea. In the area east Ras Almajdaha (at Bir-Ali district) P. margaritifera were found attached to rocks and aggregations of a variety of sponges and the coral family Mussidae; while it was absent in the most sites accompanied with Family Acropori- dae. The present observation recorded that it usually was away from aggregations of the sea urchins. It is widely distributed from Bir-Ali with large aggregation in Alhelaneah and Sekha islands. It was in moderate quantities in western Bir-Ali district. In Al-Mukalla coast it was distributed at Al-Mukalla Lagoon and Al-Mehdar rocky shore–East of Mukalla. P. margaritifera were likely absent in the coast that extended from Holiday Inn hotel (East of Mukalla) up to Alriayn area. By the way, this is probably because this site was mainly with sandy – muddy bottom and somewhat devoid of hard rocky formulations. Occasionally specimens had gath- ered in break waves of Bukhshan Factory port in Sheheer and Al shihir areas, while significant amounts were found in Fig. 3 Shell of P. margaritifera (interior side) from Hadhramout Al-Garin district, Sharma cape and Quseiar Beach. coast. Existence, growth and reproduction of pearl oyster Pinctada margaritifera 477

positive correlation (R2 = 0.982) between the biometric parameters (ShH and ShL) of P. margaritifera, with an equation of: Shell Length = 0.992; Shell height = 0.995 (Fig. 5). There was not a statistical significance (t = 1.0437) between the ShH and ShL. Relations between the shell parameters sug- gest isometric growth pattern in this species in the Hadhram- out coast, the Gulf of Aden. Hence it seems that this indicator is a traditional morphological attribute of this species in the area of spreading (Sims, 1992; El-Sayed et al., 2011). It should be noted that the maximum size (Sh H) of the recorded species in this study (180 mm) is higher than that reported elsewhere in the Indian Ocean: 154 mm from Mom- basa, Kenya (Kimani and Mavuti, 2002); 110 mm from India (Alagarswami, 1983); 125 mm from Red Sea (Elnaeim, 1984); 170 mm from Polynesia in the Pacific Ocean (Coeroli, 1983), however, it reached 230 mm in artificial culture conditions in Fig. 4 P. margaritifera specimens according to the total shell Hawaii (Rodgers et al., 2000). The mean size of our collection height in the examined samples. is 90.95 ± 0.31. The result revealed that growth rates for small sizes were more than for large groups with relatively apparent fluctuations between years which was partially due to a small quantity of samples. Growth studies showed that 34.6 mm was the mean growth rate for 2nd year, 3.7 mm for the 7th year (Fig. 6). Although our P. margaritifera reached a shell height of 180 mm but it took 7–8 years, that to speak about slow growth in comparison with this species of Kenyan and Andaman waters and under culture conditions (Alagarswami, 1983; Pouvreau and Prasil, 2001; Mavuti et al., 2009). The estimated von Bertalanffy growth parameters were ShH 1 = 170.31 mm, K = 0.41, to = 0.24. One of the constraints to the growth of the oyster is the biofouling or bio contamination on the shell, which is a vital ref- uge and base for many of the settling benthic organisms (Dharmaraj et al., 1987; Doroudi, 1996; Mohammed, 1998; Southgate and Beer, 2000). But what appeared in the present study, that more than 92% of the collected oysters were free and clean of biofouling dynamic (17 of 213 samples), therefore Fig. 5 Correlation coefficient (R2) between the biometric we cannot attribute slow growth to such causes. The reason parameters (ShH and ShL) of P. margaritifera from Hadhramout should be explored in other ecological conditions, which would coast. be the subject of subsequent studies.

Mannar, even to the Philippines (Galtsoff, 1931, 1933; Ranson, 1952; Crossland, 1957). The size structure analyses do not indicate distinct length/ age groups. However, the structure of the size of the samples demonstrated that the population of P. margaritifera in Hadhramout coast was dominated by large samples (60–120 mm, with a mean of 90.91 ± 0.44 mm; 3–5 year old), which probably represent the mature population (Fig. 4). On the other hand, scarce samples of small individuals (<50 mm), contains those individuals that belong to the relatively young population which, appears to be struggling to establish itself in the midst of the changing environment of the Gulf of Aden.

Growth and allometric relationships

The study of the growth and allometric relationships is necessary to obtain information that would be of value to resource management and effect the changing environmental conditions and pollution. Hence our obtained results show a strong Fig. 6 Growth rate of P. margaritifera from Hadhramout coast. 478 M.S. Aideed et al.

1200

1000 Sh Wt y = 0.0026x2.49 gr Body Wt R2 = 0.93

Wt, 800 Total Wt

600 y = 0.0004x2.82 R2 = 0.92 400 Total, Shell and body 200 y = 0.0003x2.67 R2 = 0.75 0 0 50 100 150 200 Shell Height, mm Fig. 8 Frequency distribution of relative size of males, females, and juvenile pearl oysters (Pinctada margaritifera) identiﬁed by Fig. 7 Correlation between shell height and total wet weight, gonadal smears examination of specimens, in Hadhramout coast. shell and soft body weight of Pinctada margaritifera in Hadhram- out coast.

with the size of individuals and it was possible to identify some Length–weight relationship specific patterns (Fig. 8). With increasing size, there is a con- stant and somehow rapid increase in the share of females in The study of the length–weight relationship is necessary to the population, so that when the size of P. margaritifera obtain information that would be of value to resource manage- exceeds 100 mm there is a sharp decline in the proportion of ment and address the changing environmental conditions and males; consequently, in this region the average life duration pollution. The present results show a strong positive correla- 2 of females seem to be higher than males. This means that it tion (R = 0.93) between the biometric parameters (total Wt is a protandric hermaphrodite species. Despite this, in general, and ShH) of P. margaritifera, with an equation of: Total it can be seen as predominance of males over females weight = 0.0026 Shell height 2.49 (Fig. 7). (M:F = 1.2:1). Such coefficient of correlation was relatively high in the 2 Latter attributions are identical to the M:F ratio of 1.29:1 case of just with shell weight (R = 0.92), but this coefficient in the Andaman, India (Alagarswami, 1983), 1.75:1 in the was comparatively low between the shell height and body South China Sea (Dolgov, 1991) and 1.3:1 in Kenya (Kimani weight – R2 = 0.75 as is presented in Fig. 7. Abraham et al. 2 and Mavuti, 2002). Though the considered sizes are different, (2007) obtained a much less ‘R – 0.60–0.78’, value for this spe- it is clear that the expression of the male sex is dominant in the cies from different Islands of the Andaman and Nicobar, for a P. margaritifera populations, although we do not find a differ- length range of 40–133 mm. Our results concerning total Wt ence in shell morphology associated with sex, but only gonad and ShH relationship were similar to those of Alagarswami coloration distinguishes sex in P. margaritifera. The latter is (1983) from Andaman Islands and Pouvreau et al. (2000c) 2 evident in the present samples. Various authors however, for farmed oysters in French Polynesia : R = 0.96 and 0.97 claimed the contrary of these results (Alagarswami, 1983; respectively. Velayudhan and Gandhi, 1987; Pouvreau and Prasil, 2001). The present findings showed, as judged by the adapted mat- Reproduction uration stages, the gametogenesis preceded during the year. Specimens in early and late maturation stages were observed Reproductive biology of pearl oysters is important for in all months of the year. The dominant proportion of ripe expected pearl farming, in order to understand the develop- mature specimens recorded in December 2009–March 2010 ment of the gonads and population dynamics in natural stocks. were females and along two periods in males – January–March Morphological description of gonads: Gonads of this species and August–October 2010. During the period December–May are located in the area between the feet and wrap, the gastro- the gonads undergo a transition to spent stages and probably intestinal tract, and around the last makes the process of keep the ability to spawn as the population quickly moves to gonad isolation so difficult, especially in the early stages of maturity stage 4 in June (Fig. 9). growth and development. There are visible spreads of gonads Such behavior has been observed in almost all of the in the area between byssal glands and stomach. Despite what populations of P. margaritifera in their distribution areas is said about the difficulty of determining gender of this spe- (Crossland, 1957; Tranter, 1958; Hwang, 2007; Pouvreau cies, our screening through gonadal tissue smeers on the slides, et al., 2000a,b) and in many of species of this genus (Rose showed the possibility of follow up of the color to a large et al., 1990; Wada et al., 1995; Arjarasirikoon et al., 2004; degree. The male’s gonads show a more light color than Garcia-Dominguez et al., 1996; Gervis and Sims, 1992). females in all stages they are always closer to the milky white P. margaritifera also can exhibit two periods of maximum while females tend to dark yellow color, first maturation stages spawning, which also can be deduced from the present study at a pink to light gray glance. (Tranter, 1958; Coeroli et al., 1982; present study). Moreover, During the study period the ratio between males and through the analysis we find what is consistent with and females has been unstable, but it showed a clear relationship support the conclusions of Pouvreau et al. (2000b) and Le Existence, growth and reproduction of pearl oyster Pinctada margaritifera 479

Fig. 9 Relative frequency of gonad maturation stages of P. margaritifera in Hadhramout coast through the period Sep 2009 to Nov 2010 for males and females.

timely information needed to explore the potential of recruitment in wild and mariculture. Our results demonstrate that the behavior of maturity stages is confirmed by the less fluctuations of the mean gonadic index (GI). Naturally, the GI of individuals was complying with that of annual character what in the maturity stages, and the data showed that GI monthly variations of males and females followed nearly the same pattern (Fig. 10). The comparison of the contents of Figs. 9 and 10 reveals three ostensible peaks and an evident decline in GI, spawning. The three, so called peaks, presumably correspond to a long phase of high maturity stages between September–November 2009 and April–November 2010 with, as we believe, some tech- Fig. 10 Gonad index through the period Sep 2009 to Nov 2010 nical interruption of data due to the lack of female sampling for males and females. (see dotted arrow in Fig. 10). A decline of GI indicated in Jan- uary–March confirmed at least one major spawning event, especially in females; especially under the high Gonad Index Moullac et al. (2012) that P. margaritifera could be defined as of males during this period (Fig. 10). an opportunistic spawner. Despite the fact that there are no previous studies on Spawning conditions usually are determined using two key P. margaritifera in the study region, the occurrence of both parameters, the practical scale of gonad, qualitative, and the adult and juvenile individuals indicates that the Hadhramout quantitative parameters, and gonadal index. They have the coastal environment is, to some extent, suitable for the growth advantage of being implemented quickly and thus ensure and reproduction of pearl oyster. 480 M.S. Aideed et al.

Biological data shown here, although seem preliminary and Coeroli, M., De Gaillande, D., Landret, J., AQUACOP, 1982. Recent stereotypical have exceptional value and anyway are the only innovations in cultivation of molluscs in French Polynesia. Int. information available about the black lip oysters in the region Symp. Cult. Pac. Molluscs. La Jolla 1–3 December. to date; and open broad prospects for the subsequent research. Colgan, D.J., Ponder, W.F., 2002. Genetic discrimination of morpho- logically similar, sympatric species of pearl oysters (Mollusca: As it appears from the general results of the present survey, Bivalvia: Pinctada) in eastern Australia. Mar. Freshwater Res. 53 the population density was low, and with our knowledge that (3), 697–709. the animal is not exposed at present and was not subjected Crossland, L., 1957. The cultivation of the mother-of pearl oyster in over the past decades to overexploitation; therefore it can be the Red Sea. J. Marine Freshwater Res. 8, 111–130. concluded that it suffers from poor survival, predation and Dharmaraj, S., Chellam, A., Velayudhan, T.S., 1987. Befouling boring poor environmental conditions, especially if it is not exploited and predation of pearl oyster. CMFRI Bull. 39, 92–97. for human consumption in the region. We believe that the Dolgov, L.V., 1991. Sex expression and environmental stress in a mollusk, upwelling that is sweeping the coast annually is one of these Pinctada margaritifera. Invertebr. Reprod. Dev. 20, 121–124. negative conditions, especially; water flow and the resumption Doroudi, M.S., 1996. Infestation of pearl oysters by boring and fouling of food are determinant factors in the growth of P. margaritif- organisms in the northern Persian Gulf. Indian J. Marine Sci. 25, 168–169. era (Pouvreau et al., 2000b; Pages et al., 2001; Pouvreau and Elnaeim, A.G., 1984. Variability in growth of the mother of pearl Prasil, 2001; Mavuti et al., 2009). 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