macroscopic and microscopic anatomy of the …keywords: reptilian, anatomy, hemipenis, snake....

25 Macroscopic and Microscopic Anatomy...JKAU: Sci., vol. 10, pp. 25-38 (1418 A.H. / 1998 A.D.)

Macroscopic and Microscopic Anatomy of the Hemipenes of the Snake Bitis arietans arietans

SALEH A. KARIM

Biology Department, Faculty of Science,King Abdulaziz University, Jeddah, Saudi Arabia

ABSTRACT. The macroscopic and microscopic anatomy of the hemipenis of the snake Bitis arietans arietans were investigated. Each hemipenis appeared as a bilobed structure. By using SEM at low magnifications, the two lobes of the hemipenis appeared to form, at the base, a sharp angle. The two lobes are provided with a well-developed arrangement of sharp, sloping spines or hooks. In general, most of the spines are directed backward.

Histologically a pleated epithelium covers the hemipenis. This epithelium is very thin at the tips of the spines, but gradually thickens as it goes basally to become continuous with that in between the spines. The above epithelium covers a special kind of fibrous connective tissue which is provided with a well developed network of venous sinuses. The spines are provided with cartilagenous cones embedded in a fibrous connective tissue. At the back of the large lobe of the hemipenis there are numerous strands of striated muscles as a continuation of the propulsar muscle.

KEYWORDS: Reptilian, anatomy, hemipenis, snake.

Introduction

Although the macroscopic and microscopic anatomy of the reptilian genital organs has been investigated by many workers[1-18], the copulatory organs especially those of squamates have received scant attention. The main study was that of Dowling and Savage[19], who used the hemipenial structure in snake taxonomy. Although the reptilian fauna of Saudi Arabia comprises a wide variety of lizards and snakes, all of the workers who carried their studies on the genital system referred only to the presence of such structures giving no more details about its anatomy. In view of this fact, the present work was carried out to give an anatomical information on the hemipenes of the snake Bitis arietans arietans which is considered as one of the dangerous snakes in the western region of Saudi Arabia.

25

26 S.A. Karim

Materials and Methods

The specimens of Bitis arietans arietans identified by Farag and Banaga[20], were collected throughout the treeding season, from early April to the end of June, from different localities in Asir mountains, in the south-west of Saudi Arabia. The males were identified by the distinct thickenings on either side of the base of the tail, just behind the cloacal aperture. After anaesthetization, the hemipenis were averted by pressing gently the base of the tail. The tail was then tied tightly, just behind the hemipenses to prevent their retraction, then washed with physiological saline solution.

For histological studies the hemipenes were carefully cut off at their bases, and fixed in Bouin’s solution and processed for sectioning, sections were cut 6-8µ m thick, and stained with the counter stain haematoxylin and eosin. Some specimens were carefully removed out and immediately fixed in clod (5ºC) formaldehyde/glutaraldehyde mixture buffered at pH 7.0 and 0.1 M sodium cacodylate for 24-30 hours. After rinsing in the buffer, the specimens were completely dehydrated with graded ethanol series, then transferred to isoamylacetate critical point dried, mounted to on aluminum stabs, coated with gold and examined with a JEOLJSM-35 scanning electron microscope operating at 10 kv.

Results

The dissecting binocular was used to examine the hemipenis. In such case, the scale over the vent was firstly lifted in order to see the external openings of the hemipenses which appeared as an elliptical apertures on either side of the proctodaeum. The hemipenes were averted from these openings, by pressing the base of the tail. Each hemipenis appeared as abilobed structure. The two lobes are not equal in length; the longer one measures about 15 mm whereas the shorter is about two-thirds of the first. By using SEM at low magnifications, the two lobes of the hemipenis appeared to make, at the base, a sharp angle (Fig. 1). Nearly, the whole surface of the hemipenis finely and irregularly placted due to the presence of a well developed venous network. The two lobes are provided with a well-developed arrangement of sharp, sloping spines or hooks, the smallest of which are present on the apical part. In general most of the spines are directed backward (Fig. 2, 3). The bilobed hemipenis (forms) a bifurcated groove the sulcus spermaticus, to transport the semen from the cloaca to its tip.

Histologically a pleated epithelium covers the hemipenis. This epithelium is very thin at the tips of the spines, but gradually thickens as it goes basally to become continuous with that in between the spines (Fig. 4, 5 & 6). In such regions, the epithelium is resting on a clear basement membrane and covered externally by a thin layers of flattened cells. In between the two layers there are three or four layers of-rounded or oval epithelial cells of a highly compact nature, each of such cells contains either a rounded or oval nucleus, which in turn contains a darkly stained nucleolus. The above epithelium covers a special kind of fibrous connective tissue which is provided with a well-developed network of venous sinuses (Fig. 7,8,9). The latter progress from centrally small, slitlike cavities to large cavities, especially at the bases of the spines which help in their erec

27 Macroscopic and Microscopic Anatomy...

FIG. 1. Scanning electron micrograph of the hemipenis of Bitis arietans arietans. Note that the two lobes are not equal in both size and length (× 4800).

28 S.A. Karim

FIG. 2. Scanning electron micrograph as above showing that the lobe of the hemipenis is provided with a well-developed arrangement of sharp, sloping spines or hooks. (× 600).


FIG. 3. High magnification scanning electron micrograph of the above in Fig. 2showing that the spine are directed backward (× 1800).

30 S.A. Karim

FIG.

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32 S.A. Karim

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34 S.A. Karim

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.

36 S.A. Karim

tion to hold the bilobed hemipenis in the female cloaca during copulation. The spines are provided with cartilagenous cores embedded in a fibrous connective tissue, the later is covered by the hemipeneal epithelium. At the back of the large lobe of the hemipenis there are numerous stands of striated muscles as a continuation of the propulsar muscle (Fig. 7, 8, 9).

Discussion

Bellaris[21]; Goin and Goin[22]; Spellerberg[23], reported that male lizards and snakes possess paired copulatory organs known as hemipenes lying on their sides of the base of the tail, behind the cloaca and in some species they form distinct thickenings which betrays the sex of their owners. This is similar to that we have observed in Bitis arietans arietans but differs from the forked hemipenis reported by Volsoqe[2] in Vipera terus and from the calyceal type observed by Goin and Goin[22], in a number of species of snakes and lizards. The hemipenis of Bitis is bilobed and the sulcus which transport the semen from the cloaca to the tip of the hemipenis is thus bifurcated. These observations agree with those of Bellaris[21] and Spellerberg[23]. The first author reported that the appearance of the hemipenis is an important factor in classification of the snakes.

The main bulk of the hemipenis of Bitis is built up of a fibrous connective, rich in elastic fibres, well provided with blood sinuses and laterally positioned cartilaenous spine. All of these structures are covered by tightly packed epithelial layers. This histological structure is greatly similar to the anatomy of the genital organs of snakes described by Dowling and Savage[19].

References

[1] Risley, P.L., Seasonal changes in the testis of the musk turtle, Stornotherus odoratus, J. Morph., 63: 301-317 (1938).

[2] Volesoe, H., Structure and seasonal variation of the male reproductive organs of Vipera terrus (L). Spolia Zool. Mus. Haunienis, 5: 5-157 (1944).

[3] Bellaris, A. and Underwood, G., The origin of snakes. Biol. Rev., 26: 193-236 (1951). [4] Fox, W., Seasonal variation in the male reproductive system of pacific garter snakes. J. Morph. 90: 481

553 (1952). [5] Fox, W., A comparison of the male urogenital systems of blind snakes, liptoyphlopidae. Herpetologica,

21: 241-256 (1965). [6] Hoge, A., Belluamini, H. and Schreiber, G., Intersexuality in a highly isolated population of snakes.

Proc. IX Int. Congr. Gentics. Caryologica, pp. 964-965 (1954). [7] Schreiber, G., Hoge, A., Belluamini, H. and Penha, A.M., Further researches on intersexuality in a

highly isolated population of snakes. Prox. X Int. Congr. Genetics. Caryologica, pp. 454-456 (1959). [8] Mayhew, W.W., Comparative reproductive in three species of the genus Uma. In Lizards Ecology

(W.C. Milstead, ed.) University Missouri Press, Missouri, U.S.A., 45-61 (1967). [9] Mayhew, W.W., Reproduction in the desert lizard Dipsosaurus dorsalis. Herpetologica, 27: 57-77

(1971). [10] Underwood, G., A contribution to the classification of snakes. Monogr. Brit. Mus. Nat. Hist. Land. 653:

1-179 (1967). [11] Smith, R.E., Experimental evidence for a gonadal fat body relationship in two teiid lizards (Ameiva

festiva, Ameiva quadrilineata). Biol. Bull. Mor. Biol. Woods Hole, 134: 325-331 (1968). [12] Mayhew, W.W. and Wright, S.J., Seasonal changes in testicular histology of three species of the liz

ard genus Uma. F. Morph., 130: 163-183 (1970).


[13] Amer, F.I., Seasonal variations in the testis and epididymis of the aquatic snake, Natrix tesellata. Ann. Zool. XI(3): 97-111 (1976).

[14] Farag, A.A. and Hashem, M., Comparative histology of the gonads in Mabuya quinquetaeniate and Ag-ama stellio. Ann. Zool. XVI, 4: 151-167 (1980).

[15] Farag, A.A., Comparative histology of the male gonads in the lizards, Uromastyx philbyi and Mabuya brevicollis. Ann. Zool., XX(2): 59-70 (1984).

[16] Rajab, M.O., Urogenital system in some squomates at the western region of Saudi Arabia. M.Sc. Thesis. Department of Biology, Faculty of Science, K.A.U. (1996).

[17] Sait, H.S., Comparative histological studies on productive system on three reptilians from western region of Saudi Arabia. M.Sc. Thesis Dept. Biology, Faculty of Science, K.A.U. (1997).

[18] Hantoush, S.M., Anatomical studies on the urinogenital system in some lizards. M.Sc. thesis. Department of Biology, Faculty of Science, K.A.A. (1998).

[19] Dowling, H.G. and Savage, J.M., A guide to snake hemipenis. Zoologica. N.Y., 45: 17-28 (1960). [20] Farag, A.A. and Banaja, A., Amphibian and reptiles from the western region of Saudi Arabia. Bulletin

of the Faculty of Science, K.A.U., 4: 5-29 (1980). [21] Bellaris, A., The Life of Reptiles, vols. I, II. Universe Books. New York (1970). [22] Goin, C.J. and Goin, O.B., Introduction to Herpetology. W.H. Freeman Co., San Francisco and Lon

don (1971). [23] Spellerberg, I.F., Biology of Reptiles, Blackie London, Glascow (1982).

38 S.A. Karim

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39 Study on Freshwater Fish Fauna...JKAU: Sci., vol. 10, pp. 39-45 (1418 A.H. / 1998 A.D.)

Study on Freshwater Fish Fauna of the Mid-Western Region of Saudi Arabia

HAMID S. AL-GHAMDI and O.A. ABU-ZINADAH

Biol. Sciences Dept., Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia

ABSTRACT. Eight localities were chosen for this study, three in the lowlands of Tihama and five in the high lands of Hijaz Mountains. In these localities four species of fishes were found, Aphinus dispar, Cyprinion acinaces, Garra buettikeri and Cyprinion mhalensis. The first two were found in the low lands while the other two were in the high lands of Hijaz.

Introduction

Fish live in virtually all kinds of aquatic habitats and have developed a wide variety of form and function. Freshwater habitats have a fragile nature, which in the last few decades in developing regions is subjective to intensive environmental pressures affecting fish habitats and populations.

Freshwater fishes from different parts of Arabia have been described by Boulenger[1], Trewavas[2], Fowler and Steinitz[3] and Balleto and Spano[4]. The most comprehensive work on freshwater fishes from Saudi Arabia and Arabian Peninsula, was carried out by Al-Kahem and Behnke[5] and Krupp[6], Banister and Clarke[7]. In addition. Ross[8] has listed one secondary freshwater species, ten marine species found in drainage system and seven introduced species from seven oases in the Eastern Province of Saudi Arabia.

Al-Kahem and Behnke[5], Krupp et al.[9], Maitland and Campbell[10] have emphasized the importance of further studies on freshwater fishes, their habitats and their distribution before extinction caused by human activities. This will provide baseline data for a long-term monitoring of ecological changes and thus for a meaningful assessment of human impact, which is a prerequisite to the implementation of conservation policy.

Many freshwater fishes distributed throughout the Mid-Western Region of Saudi Ara-bia,drought and human activities affecting surface water in the area suggest that it is necessary to undertake this study.

39

40 H.S. Al-Ghamdi & O.A. Abu-Zinadah

Materials and Methods

a) Fish Samples

During field studies on the ecology of some freshwater habitats in the Mid-Western of Saudi Arabia by Al-Ghamdi et al.[11], a total of 279 fish specimens were collected by different types of net and line. Collected fishes were preserved in 10% formalin solution and were additionally injected with formalin for future taxonomic studies. Fish identification has been checked by Dr. F. Krupp, during his participation in a symposium on Red Sea Marine Environment organized by Faculty of Marine Science, K.A.A.U., Jeddah, Saudi Arabia in 1994.

b) Study Area

The Mid-Western Region of Saudi Arabia extends from the Red Sea including the low lands of Tihama Plateau and the high lands of Sarawat Mountains, which differ very much in their climatic and environmental conditions. It contains a large number of Wadis which can be very steep and narrow or very wide and flat. Most of the Wadis are rich in surface water all year round, some other Wadis contain surface water for few months after rainy season or may become dry for several seasons. Many dams have been constructed in the area which may alter the ecological conditions and possibly enhance the freshwater animals including fish.

Eight habitats, which had surface water at the time of this study, were chosen three in the low lands and five in the high lands (Map 1). The areas studied in the low lands are: Al-Hakak, Al-Khawar and Al-Ahsabah, and the studied areas in the high lands are: Al-Kharrar, Wadi Bowa, Zahran, Al-Habaka and Al-Ganabain.

Results

Four species of freshwater fishes were identified from eight localities studied in the low lands of Tihama and the highlands of Hijaz Mountains.

The studied localities had different types of habitats, perennial streams, intermittent streams of reservoir of dam. Three of them in the low lands and five in the high lands (Tables 1 & 2). The high lands of Hijaz differ very much from the low lands in the temperatures, salinity, etc. which play a major role as limiting factors.

Aphinus dispar and Cyprinion acinaces were found in the localities of the low lands and were not found in high lands during this study. A. dispar was collected from three localities (Al-Hakak, Al-Khawar and Al-Ahsabah), while C. acinaces were collected only from Al-Hakak.

Garra buettikeri and Cyprinion mhalensis were collected from the high lands localities only. G. buettikeri was found in Al-Kharrar, Al-Ganabain, Wadi Bowa and Al-Habaka, while C. mhalensis was collected from Al-Kharrar, Al-Ganabain and Zahran (Table 1 & 2).

41 Study on Freshwater Fish Fauna...

FIG. 1. Map of the study area.


TABLE 1. Name and type of studied habitats.

Sampling localities Type of habitats No. of specimens

(A) In the low lands:

1. Al-Hakak Perennial stream 52 2. Al-Khawar Intermittent stream 17 3. Al-Ahsabah Perennial stream 64

(B) In the high lands:

4. Wadi Bowa Intermittent stream 56 5. Zahran Reservoir of dam 13 6. Al-Kharrar Intermittent stream 14 7. Al-Habaka Intermittent stream 26 8. Al-Ganabain Intermittent stream 37

279

TABLE 2. Identified fish species and their localities.

Identified fish species Locality No. of specimens

(1) Aphanuis dispar 1. Al-Hakak (L) 17 (Ruppell, 1828) 2. Al-Khawar (L) 17

3. Al-Ahsabah 64

(2) Garra buettikeri (Krupp, 1983)

1. Al-Kharrar (H) 2. Al-Genabain

(H) 3. Wadi Bowa (H) 4. Al-Habaka (H)

3 2

56 26

(3) Cyprinion acinaces (Banister & Clarke, 1977)

1. Al-Kakak (L) 35

(4) Cyprinion mhalensis 1. Al-Kharrar (H) 11 (Al-Kahem & Behnke, 1983) 2. Al-Genabain 35

3. Zahran 13

(L: Low land, H: High land)

Discussion

Krupp[6] pointed out that habitats for freshwater fishes is limited in Arabia. Freshwater offer fish as many different possibilities of life as does the sea. It is no wonder then that the fish living in a cool mountain brook are not also found inhabiting a peat-pit in the low lands, the types of habitat available are therefore of considerable interest[12].

Only about ten species have so far been described from Arabia. The situation is mainly to be attributed to the arid climate. Fishes are largely restricted to higher altitudes where precipitation is higher than in the low lands[6].

In this study Aphinus dispar and Cyprinion acinaces were found in the habitats of the low lands of Tihama, while G. buettikeri and C. mhalensis were found in the habitats of the high lands of Hijaz Mountains.


A. dispar is widely distributed between N.E. Africa and N.W. India living under freshwater, brackish or marine conditions[8]. This species appears to be most widely distributed species in Arabia. This distribution is due to its adaptation to extreme temperatures and salinity. Additionally, its feeding habits allow it to colonize extreme hab-itats[6,13,14] characterized this species as an opportunistic omnivore. This species has been introduced for mosquito control in some artificial water bodies in Oman[13].

C. mhalensis is known only from the Rub’al Khali basin and C. acinaces from western and southern coastal drainage[5]. C. mhalensis and C. acinaces appear to be closely related to each other, probably forming sibling species[5,6]. According to Howes[15] the endemic Arabian species C. acinaces retains the most primitive characters of all species in the genus. G. buettikeri occurs in the streamlets of the Eastern Asir range (at an altitude of 1400-2400 m above sea level) which drain towards the Wadi ad-Dawasir. This pattern of distribution is shared by C. mhalensis and Barbus apsensis[6]. G. buettikeri shares morphometric characters with G. tibanica and with African Garret[6].

Cyprian gazes on plant material, and is able to cut filamentous algae,while Garret ingests loose organisms and detritus from the surface of the sand and stones, together with inorganic matter. These two modes of feeding are obviously very successful in arid ar-eas[13].

Further work is needed in other parts of the country to complete the picture. Freshwater fish fauna of Saudi Arabia and to correlate the presence of these species and their morphological, anatomical and behavioral adaptability to the surrounding environment. Shulz et al.[16] have started some work on freshwater fishes of Wadi Turabah, Saudi Arabia which needs to be extended to other parts of Arabia.

References

[1] Boulenger, G.A., An account of the fishes obtained by A. Jayakar at Muscat, east coast of Arabia. Proc. Zool. Soc. London: 653-667 (1887).

[2] Trewavas, E., Freshwater Fishes. In: Br. Mus. (Nat. Hist.), Expedition to South-West Arabia. 1937-8, 1: 7-15. London (1941).

[3] Fowler, H.W. and Steinitz, H., Fishes from Cyprus, Iran, Iraq, Israel and Oman. Bull. Res. Counc. Israel, 5B: 260-292 (1956).

[4] Balleto, E. and Spano, S., Ciprinidi del genere Garra Hamilton, 1822 raccolti nello Yemen dal Prof. Giuseppe Scortecci. Ann. Mus Civ. Stor. Nat. “Giacomo Doria,” 81: 246-287 (1977).

[5] Alkahem, A.F. and Behnke, R.J., Freshwater Fishes of Saudi Arabia, Fauna of Saudi Arabia, 5: 545567 (1983).

[6] Krupp, F., Freshwater Fishes of Saudi Arabia and adjacent Regions of the Arabian Peninsula. Fauna of Saudi Arabia, 5: 568-638 (1983).

[7] Banister, K.E. and Clarke, M.A., The Freshwater Fishes of the Arabian Peninsula. J. Oman Studies, Special Report: The Scientific Results of The Oman Flora and Fauna Survey 1975: 111-154 (1977).

[8] Ross, W., Oasis Fishes of Eastern Saudi Arabia. Fauna of Saudi Arabia, 7: 303-317 (1985). [9] Krupp, F., Schneider, W., Nader, I.A. and Khushaim, O., Zoological Survey in Saudi Arabia, Spring

1990. Fauna of Saudi Arabia, 11: 3-9 (1990). [10] Maitland, P.S. and Campbell, R.N., Freshwater Fishes of the British Islet. Harper Collins Publishers,

London, Glasgow, Sydney, Toronto (1992). [11] Al-Ghamdi, H.S., Al-Robai, A. and Ghandour, A.M., Ecological studies on some Freshwater Habitats

in the Mid-Western Region of Saudi Arabia. J.K.A.U.: Edu. Sci., 6: 59-70 (1993).


[12] Muus, Brent, J. and Dahlstrom, P., Collins Guide to the Freshwater Fishes of Britain and Europe. By Collins Sons and Co. Ltd. (1971).

[13] Krupp, F., Freshwater Fishes of Wadi Batha Drainage. J. Oman Studies, Special Report, 3: 401-404 (1988).

[14] Haas, R., Notes on the ecology of Aphanius dispar (pisces, cyprindontide) in the Sultanate of Oman. Freshwater Biology, 12: 89-95 (1982).

[15] Howes, G., Anatomy and evolution of the jaws in the semiplotine carps with a review of the genus cyprinion Heckel, 1843 (Teleostei: Cyprindae). Bull. Br. Mus. Nat. Hist. (Zool.), 42: 299-335 (1982).

[16] Schulz, H. and Gaucher, M.P. and Eichacker, X. (1990) Freshwater Fishes of Wadi Turabah – Water parameters, Distribution and Morphometrics. 1st. Intern. Report of the N.W.R.C. Research Project “Biology of Saudi Arabian Freshwater Fishes.”(1990).


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47 Ecological Behavior and Biology of...JKAU: Sci., vol. 10, pp. 47-72 (1418 A.H. / 1998 A.D.)

Ecological Behaviour and Biology of the Beach Clam Donax faba (Gmelin) from the Red Sea

ALI A. ESHKY

Faculty of Marine Science, King Abdulaziz University, Jeddah, Saudi Arabia

ABSTRACT. The distribution of wedge clam Donax faba (Gmelin) in the Red Sea and the offshore islands is restricted to sheltered sandy beaches between tide marks. The present investigation has shown that Donax faba does not exhibit a tidal or semilunar migratory pattern as most members of this genus but rather a seasonal migratory pattern, which is related to the seasonal changes in the sea level. A peak density occurred in November with 296 m–2 and the lowest in January with 30 m–2. Growth rate of wedge clams exhibits different seasonal patterns of growth. The greatest increase in growth rate took place in summer. It is evident from this study that Donax faba has a prolonged breeding period with two different peaks of spawning; the small peak taking place in June and the large one in November and December. These two reproductive cycles corresponded to the phytoplankton peak which occurred at the same period.

Introduction

The distribution of the bivalve Donax faba along the east coast of the Red Sea and the offshore islands is restricted to sheltered bays. It only occurs between tidal marks where the sand is usually coarse and moderately sorted[1,2]. Smith[13] and Alagarswami[4],

however, noted its occurrence on exposed sandy beaches of Africa and India respectively. The littoral environment of the Red Sea is characterized by wide diel tem-peratures[5-8]. Salinity is also high in the Red Sea and may reach 41% in the reef pools in the Jeddah region in July and August[5]. Temperature may rise above the upper lethal limits of the littoral fauna[8] and it seems unlikely that the lower lethal limits will ever be reached in the study region. Not much information is available regarding different aspects of studies of Donax faba. Hodgkin[9] reports that extreme environmental temperature most likely affects the population level of the gastropod Dicathais aegrota in Western Australia. Eshky[10] has also found that extreme high temperature and extreme low relative humidity could also have the same effect on the brachyuran crabs Uca species during the summer in the Jizan region.

47

48 A.A. Eshky

In the Jeddah region the maximum spring tide range is about 36 cm[5,6,11,12], but despite its small magnitude it plays an essential role in the behavior of littoral fauna particularly on the feeding behavior[6-10].

There is a marked seasonal variation in mean sea level in the Red Sea which is related to the monsoon winds in the Indian Ocean[5,11,12,13]. Tidal migrations were reported for Donax faba by both Smith[3] from the east coast of Africa, and by Al-agarswami[4] from Mandapam coast of India, and also from other localities[14-19]. Prosch and Maclachlan[20] have also suggested that different size classes of Donax serra show different patterns of movement. However, in the present study, Donax faba neither exhibited tidal pattern nor a semilunar migratory pattern but rather a seasonal migratory pattern related to the seasonal variation in the mean sea level. Similar patterns of behavior were observed for semi-terrestrial crabs[6-8,10].

The growth rate of Donax faba were investigated by Alagarswami[4] and of other members of the same genus by several workers[21-24]. Quayle[25] and Auger[26] related the slow summer growth rate of Pacific oyster Crassostrea gigas to spawning activity. Mori et al.[27] have reported similar conclusions.

Variation in the timing of gametogenesis and spawning have also been documented among several populations of bivalve molluscs[28,29] but the causes of this variability are not understood. Differences in environmental temperature and salinity[4,21,30], seasonal abundance, and composition of food[31-33, 28, 34, 35] are thought to affect the reproductive cycles of marine invertebrates. The present study investigates the effect of environmental variables on the distribution of the wedge clam Donax faba. Allometric and growth rate of the clams were also investigated in addition to the causes of variation in timing of reproduction.

Methods

Field work was carried out on the south side of Sharm Obhour (an inlet), 21º42′26″N and 39º06′06″Ε adjacent to the Marine Station of the Faculty of Marine Science, King Abdulaziz University. The beach is privately owned with minimal human disturbance. A large population of the wedge clam Donax faba was found in a very narrow strip along the beach between the average mean sea level and the extreme winter high watermark. The study area was surveyed using a Wild To5 theodolite surveying device to measure the beach profile and sea level. Monthly field data were collected between April 1994 and March 1995. The study site is illustrated in Fig. (1). Its landward side is a flat sandy beach occupied by the ghost crabs Ocypode saratan while seaward is narrow lagoon behind the coral fringe of Sharm Obhor. This lagoon is only 5-20 m wide and less than 2 m in depth and is superficially muddy. The coral fringe is very rarely exposed to air due to monsoon effect in summer. For laboratory investigations the clams were obtained from Al-Guaid Island which is located about 35 km north of Sharm Obhor. Clams were collected using a frame quadrat 25 × 25 cm forced into the sand to a depth of approximately 20 cm until reaching the hard substratum. All sand including the wedge clams inside the frame were sieved through a 2 mm mesh sieve to collect the

49 Ecological Behavior and Biology of...

FIG. 1. Map showing the study location.

50 A.A. Eshky

clams. Their dimensions were measured to the nearest 0.1 mm using vernier caliper. A digital thermometer (R.S. components) connected to thermo-coupling wires was used to monitor temperature changes in various microhabitat occupied by the wedge clams. Water salinity was measured by hand refractometer (Alago). Coded plastic label tags of different size were used depending on the size of the animals. Each label had a plastic extension on the back of each tag and were attached to the shells by drilling a fine hole of about 0.6 mm (using precision drill R.S. components) through the shell and inserted into the drilled hole and cemented together with the tag by cyanoacrylate glue on the clam shell. Sediment cores were taken for granulometric analysis at depth of 15 cm from three different stations along the wash zone where the clams were found. Sediment analysis followed methods detailed by Folk and Gray[36-37]. Population density of Donax faba was determined by placing a grid of 1 m × 10 m which cover the narrow strip occupied by the clams.

On each visit the beach was surveyed using the thediolite, so that the position of the clams could be related to the tidal datum. Clams were collected, counted, and mapped on graph paper with reference to the established datum point.

For histological study the specimens were narcotized using a saturated solution (7.5%) of magnesium chloride (MgCl2) which gave satisfactory results. The shells of the wedge clam Donax faba were opened and the soft tissues of the animals withdrawn from their valves. The narcotized specimens were fixed in alcoholic bouins solution for a period varying from 24-48 hours, thereafter they were washed several times in 50% ethyl alcohol until their yellowish coloration disappeared, and finally preserved in 70% ethyl alcohol for further histological study. Afterwards, the preserved specimens were dehydrated through successive series of ascending concentrations of ethyl alcohol 80%, 90%, 95% and 100% twice. The dehydrated specimens were passed through a series of a mixture of paraffin wax and xylene (1:2) and left for 30 minutes, then transferred to another mixture of paraffin wax and xylene (1:1) and left for an hour, then they were put in a mixture of paraffin wax and xylene (2:1) for one and half hour respectively. Finally, the tissues were embedded into three successive series of pure melted paraffin wax (melting point of 58-60ºC) for at least two and a half hours. The embedded specimens were cut by using a rotary hours. The embedded specimens were cut by using a rotary microtome into serial sections with a thickness of 5-7 micron. Horizontal and transverse sections were made and stained by Ehrlich Heamatoxylin eosin stain which gave an excellent result. Finally, the stained sections of the specimens were examined by a light microscope.

Results

Distribution

The general distribution of Donax faba is poorly known and there have been no previous attempts to investigate ecological variables controlling their distribution in the Red Sea. Therefore, in addition to the two major study sites the wedge clams were collected from three different beaches throughout the east coast of the Red Sea and some

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offshore islands in the south and the middle region of Red Sea. These locations were at the west coast of Farasan island 850 km south of Jeddah and Al-Iga island located just 8 km west of Al-Guaid island. In all different locations the distribution of Donax faba populations are restricted to sheltered sandy beaches along the east coast of the Red Sea and offshore islands which are both protected by the fringing reef. Donax faba occurred in abundance in narrow waterlogged sandy strips. The extent of this strip varies with beach slope and sand grain size which is usually coarser sand with phi values ranging between 1.2 to 1.45. The fine grain size of the muddy lagoon at Sharm-Obhor site and the exposed coral platforms of Al-guaid island prevent colonization of Donax faba in such areas. Also the population distribution of Donax faba varies seasonally with variation in the mean sea level due to the monsoon effect.

Population Density

Analysis of the samples through the 10 m grid along the narrow zone occupied by the clams indicates that the density of the population at different squares within the grid varies appreciably between a maximum of 742 m–2 and a minimum of 0 m–2. This reflects the great deviation of the population density from the population mean (Table 1). Also, there were appreciable monthly fluctuations (Fig. 2).

TABLE 1. Monthly variations in population density of Donax faba.

Month Mean density numbers m–2 Standard deviation (sd) Pattern

Apr 119.25 143.89 Clumping May 133.25 204.2 Clumping Jun 135.00 173.13 Clumping Jul 160.5 172.50 Clumping Aug 151.75 161.70 Clumping Sep 197.5 151.13 Clumping Oct 181 113.25 Clumping Nov 296 350.1 Clumping Dec 166 59.05 Clumping Jan 29.25 34.07 Clumping Feb 53.25 65.18 Clumping Mar 46 41.7 Clumping

The greatest population density was recorded in November 1994 with 296 individuals per square metre and the lowest in January 1995 with 30 m–2. However, the twelve annual distributions were clumped with P < 0.001 obtained from the dispersion equation

X2 = S2 (n – 1) where n = number of samples X2 = coefficient of dispersion × S2 = – x –variance and x = the population mean.

In winter months particularly January, February and March, the beach is usually exposed to strong wave action due to stormy weather. As a result, the individuals of Donax faba are carried far away up the beach and most of them eventually die. The mortality rate during this period may be as high as 52%. The reduction of the population

52 A.A. Eshky

density of Donax faba in January to March due to the rising sea level and relatively strong wave action which occasionally flushes out the clams out of the sand and deposits them so high up on the beach that they never regain their proper zonation. In such cases a high mortality of 52% in December, January and February respectively of tagged clams was recorded.

FIG. 2. Histograms of monthly variations in population density of Donax faba.

Substratum Characteristics

Grain size is considered to be a limiting factor on the distribution of Donax faba. Little variation in the size of sediment grains was recorded at the three stations and, phi values ranged only from 1.2 to 1.45 (Table 2). The negative skewness (Fig. 3) shows an over abundance of coarse grains which are moderately sorted in the three stations.

TABLE 2. Characteristics of the sediment in the study site.

Station Depth of core

(cm)

Mean particle diameter

φ

Sorting coefficient

φ Description

1 0 - 15 cm 1.12 1.054 moderately sorted 2 0 - 15 cm 1.45 1.003 moderately sorted 3 0 -15 cm 1.15 1.012 moderately sorted

Temperature and Salinity

Sea water temperature and salinity observations were taken monthly between 1200 h. and 1400 h. and are summarized in Fig. (4).

On 25th of July 1995 the beach was visited and a series of measurements was conducted over an 18-hour period, tide was spring tide. During the ebbing tide which took


FIG. 3. Grain size data of the study location 1, 3 top and lower of the wash zone respectively, 2 is the middle zone.

54 A.A. Eshky

FIG. 4. Monthly variation in water temperature and salinity.

place around 12:30 h by this time Donax faba zone was exposed to direct sunlight. At this time the sand surface temperature showed the greatest diel variation which reached 39.8ºC and dropped to 29.5ºC during the next ebbtide which occurred at 24:30 h. The low nocturnal temperature of the beach presumably reflects flooding of the clam zone by cold surface water at night either by the moderate waves or by the high tide which started to cover the clams zone at 24:30 h. Temperature profiles (Table 3) were taken through the sand on two occasions, at 12:30 h and 24:30 h during ebbtide, at 12:30 h the sand surface was relatively dry due to sun evaporation whereas at 24:30 h the sand surface was very heavily waterlogged as a result of successive moderate waves which un


usually occurred at this time. Air temperature at 12:30 h. was 38ºC, surface water temperature was 28.5ºC and sand surface temperature 39.8ºC. A difference of 11.5ºC between sand surface temperature at 12:30 and 24:30 h was noted. But, at a depth of 15 cm through the clams’ zone the temperature was similar.

TABLE 3. Sand temperature (ºC) profile at different depths on the wash zone during the ebbtide 25th of July 1995.

Depth Temperature (cm) 12: 30 h 24:30 h

0 39.8 28.5 5 37.7 27.9

10 30.9 27.9 15 28.1 27.9 20 28.1 27.9

Tide

No accurate continuous tidal records exist for the study region. Limited data on tides were obtained during the present study which clearly show the tide is semidiurnal and of small amplitude. The data illustrated in Fig. (5) were personally obtained at the study site by manually measuring the tidal rise and fall in relation to a reference point. The tidal range varies from 10 cm to around 30 cm.

FIG. 5. Spring and neap tide range at the study site.

Mean Sea Level

There is a remarkable seasonal variation, in the mean sea level in the Red Sea due to the monsoon effect[5-8,12,13,38]. Patzert[12] suggested that the monsoon wind reversal is the major factor controlling sea level. Morley[5] summarized this by indicating that during the winter monsoon, predominantly SSE winds drive the surface waters of the Gulf of Aden northwards into the Red Sea. This inflow exceeds losses due to evaporation and subsurface outflow and results in increase sea level particularly between 19ºN and 25ºN where the current opposes the NNW wind of the northern Red Sea. Mean sea level

56 A.A. Eshky

gradually falls from January to late July. When monsoon reversal is complete the NNW winds blow throughout the Red Sea, there is a net loss of water, reducing mean sea level to an August minimum after which sea level gradually increases. Morley’s own data were recorded 10 km north of Jeddah and demonstrated dramatic short term coastal sea level fluctuations caused by transient changes in wind direction. Koenig[38] however, considers in a computer model that surface circulation is mainly driven by the pressure gradient caused by the density field and not by the wind.

Whatever the factors controlling circulation are, the resulting sea level changes were clearly observed by Eshky[6-8] who recorded the seasonal variation from Jizan city, 750 km south of Jeddah and from the same area where Morley[5] recorded his data. The present study clearly illustrates the seasonal change in the level (Fig.6) and is in full agreement with all previous studies. However, the mean sea level in the present study is not the true mean and standardized to the tidal cycles, but represents the height of sea level to a standard point at each period of observation.

Tidal Migration

At the study site the maximum height of both spring tide and meap tide never exceeds 35 cm and 10 cm respectively. The beach is relatively flat having a slope of 1:15. The fall water level on both low spring tide and low ebbtide is not sufficient to cause any potential desiccation danger to the clams. The exposed area during low tide is characterized by always having continuous slick of water on its surface from the successive small waves which have a frequency of around once every 40 seconds or more. Therefore, the study of zonation of tagged Donax faba to the related datum point revealed that the clams remained quiescent in the sand during low tide, and there was no evidence to suggest tidal migration of this species on the beach. On the other hand the position of the wedge clams Donax faba is highly affected by the seasonal variation in the mean sea level where the position to clams on the beach varies seasonally, Fig. (6).

FIG. 6. The seasonal variation in the vertical distribution of Donax faba.


In winter months (December-March) the wedge clams start to leave the sediment and move up the beach in response to the rising sea level. During the summer months (April-November) the wedge clams respond to the fall in of the ground water table by moving to the sand surface where they were carried down the beach by the back wash and burrowed in the saturated sand. Due to the small size, the wedge clams may easily be carried up and down the beach with the advance the backwash of small waves which usually occurred at the study site. The responses of Donax faba to the seasonal rising and falling of the mean sea level and hence the vertical seasonal tidal migration is likely to be endogenous.

Shell Dimensions

Relationship between linear dimension of shell length (L), shell height (H), shell thickness (TH), and shell total weight (W) for the Donax faba population from Sharm Obhour (SO) and Al-quiad Island (AI) are shown in Fig. (7) and linear regression values are summarized in Table (4).

FIG. 7. Relationship between linear dimension versus total weight of Donax faba shells from both sites.

In each case, the regression line is highly significant (P < 0.001). Employing shell length as a reference dimension, this study has demonstrated that within the average of 7.1 to 31.61 mm of shell length, all different dimensions were growing strictly iso-metrically. Similar results were obtained if shell height, shell thickness or shell total weight were employed as a reference dimension. Covariance analysis showed that there were no significant differences in the shells’ dimensions between both sites (Table 5).

There does not appear to be any phenotypic variability in shell shape variables at the two different site.

Specific Growth Rate

A total of 150 clams were captured tagged and released. On subsequent visits the release site was searched for tagged clams. Length at release and new length were noted

58 A.A. Eshky

for all tagged individuals, to compare and analyse the growth during different seasons. Monthly instantaneous growth rate were calculated using the following formula of Win-berg[39].

G = log10 L2 – log10 L1

t

where L1 and L2 are the lengths at the beginning and the end of the experiment, respectively, and t the duration of the experiment in months. G was then plotted against log10 initial length for each season. May 1994 is considered to be the initial length for summer, August for fall, November for winter and finally February for the spring. The regression equation of the lines fitted to all data are represented in Table (6).

TABLE 4. Regression statistics of linear shell dimension and total weight of Donax faba from Sharm Obhour (SO) and Al-quiad Island (AQ).

Site log y = log a - b log x r n

SO (L - W) log y = – 4.96 – 4.01 log x 0.84 46 AI (L - W) log y = – 4.82 – 3.97 log x 0.95 46 SO (L - H) log y = – 0.238 – 1.33 log x 0.99 102 AI (L - H) log y = – 0.25 – 1.41 log x 0.99 102 SO (L -TH) log y = – 0.56 – 1.16 log x 0.99 102 AI (L - TH) log y = – 0.57 – 1.15 log x 0.99 102 SO (TH -W) log y = –3.18 – 3.61 log y 0.99 102 AI (TH - W) log y = – 3.13 – 3.55 log y 0.94 102 SO (H - W) log y = – 4.28 – 3.67 log y 0.88 102 AI (H - W) log y = – 4.19 – 3.58 log y 0.95 102 SO (H - TH) log y = – 0.311 – 1.02 log y 0.99 102 AI (H - TH) log y = – 0.295 – 1.01 log y 0.99 102

TABLE 5. Covariance comparisons of different shells dimensions, length (L), weight (h), thickness (th) and total weight from the two sites.

Compared groups df P

L (SO) - L (AI) 205 NS P > 0.98 H (SO) - H (AI) 205 NS P > 0.96 TH (SO) - TH (AI) 205 NS P > 0.97 W (SO) - W (AI) 39 NS P > 0.41

TABLE 6. Regression equations for seasonal length specific growth rate (G) against log10L1.

Season log y = log a - b log x n r

Summer log y = 0.24 – 0.009 log x 9 0.99 Fall log y = 0.13 – 0.005 log x 9 0.95 Winter log y = 0.114 – 0.004 log x 9 0.91 Spring log y = 0.117 – 0.004 log x 9 0.98

In each case, the regression line is highly significant (P < 0.005).


Covariance analysis of these data showed significant differences in both the slope (b) and the elevation (a) of the regression lines of the specific growth rate between summer and the remaining seasons, where there was no significant difference in the slopes (b) or the elevations (a) of the regression lines of the specific growth rate between the remaining seasons.

The negative slopes of the regression lines indicated that juvenile clams grow faster than adult clams. Also the elevations (a) of the regression line showed a remarkable increase in the growth rate in the summer compared to the remaining seasons.

TABLE 7. Covariance comparisons of seasonal specific growth rate of Donax faba.

Compared groups a b

Summer – fall S (P < 0.005) S (P < 0.005) Summer – winter S (P < 0.001) S (P < 0.001) Summer – spring S (P < 0.001) S (P < 0.001) Fall – winter NS NS Fall – spring NS NS Winter – spring NS NS All combined S (P < 0.005) S (P < 0.005)

Reproduction

The wedge clam is a diocious organism. The reproductive cycle[4,40,41] is divided into the following: active, mature, spawning – (divided into partially and completely spawned) and the resting stage. Oogenesis and spermatogenesis can be distinguished in the gametogenic processes. Monthly mean diameter of oogenic and spermatogenetic elements were determined. Values on the development of the male and female gonads of Donax faba (Table 8) indicate an increasing pattern on the oogenic and spermatogenic elements.

TABLE 8. Development of female and male gonads in D. faba (Gmelin).

Month

Mean percentage of oogenic elements

Mean diameter of oogenic

elements (µm) Stand. dev. ±

Mean percentage of spermatogenic elements

April 0.18 4.70 0.88 1.73 May 2.93 32.4 7.21 5.34 June 6.87 47.63 7.44 15.41 July 2.52 18.75 5.22 22.19 August 11.44 9.66 5.61 17.01 September 11.97 37.5 3.83 13.86 October 13.09 42.89 6.68 12.01 November 16.48 45.5 7.08 9.39 December 13.92 53.0 4.57 2.28 January 10.46 55.5 4.98 0.0 February 1.46 3.25 0.72 0.0 March 8.24 4.35 0.79 0.78

60 A.A. Eshky

Spermatogenesis

Spermatogenic activities in Donax faba were observed from April 1994 to March 1995. Observed characteristics of the spermatogonial cells are as follows:

(a) Activation Stage Plate (1). In April, testes were located nearly at the dorsal part of the foot, occupying a small area. Oval and circular nuclei embedded in oval follicles filled with vesicular connective tissue. Definitive spermatogonial cells aggregated in small groups at the centre of follicles with mean diameter of about 4.1 µm.

PLATE 1. Activation stage in male (H.S.) showing (1) vesicular connective tissue, (2) definitive spermatogonial cells, and (3) nucleus.

(b) Maturation Stage Plate (2). Early stage of maturation began in May. Reproductive follicles showed different stages of spermatogenic elements (e.g. stem cells, secondary spermatogonial cells). Primary and secondary spermatocytes are clearly seen occupying the central part of the follicles.

June, the clams were already in advanced stage of maturation. Spermatids and sperm were seen clearly occupying most part of follicles. In July, all clams were found in the full ripe phase, gonadal follicles filled with huge numbers of sperm while their tails were extended towards the center of the follicles.

(c) Spawning Stage. August, gonadal follicles showed different degrees of emptiness, an indication that sperm were reduced gradually [Plate (3)]. Follicular diameter began to decrease in size and intrafollicular spaces were seen easily.


PLATE 2. Stage of maturation in male (H.S.) showing (1) secondary spermatocytes cells, (2) primary spermatocytes (H.S.), and (3) stem cell (H.S.).

PLATE 3. Early stage of spawning in the male (T.S.) showing (1) intrafollicular space and (2) ripe sperms.

62 A.A. Eshky

September, marked the continued intensive spawning where large number of fully matured spermatozoa filled the follicles. Intrafollicular spaces increased in size. In October, partial emptiness of gonadal follicles was observed indicating partial spawning and in November, reduction of ripe sperm was very distinct and both inter and intra-follicular spaces increased. In December, ripe sperm reached their minimum while few follicles were ruptured, others retained their forms. Relict sperm were found inside the gonadal follicles.

(d) Resting Stage, Plate (4). January, gonadal follicles were completely devoid of sperm. Phagocytic cells present in large numbers all over the follicles. Vesicular connective tissue rebuilding and transparent.

PLATE 4. Resting stage in male (T.S.) showing (1) phagocytic cells, (2) gonadal follicles and (3) vascular connective tissues.

In February, vesicular connective tissue gradually losing its transparency indicating an active formation of forthcoming reproductive cycle.

(e) Activation Stage Plate (5). In March, oval nuclei of vesicular connective tissue appeared. Small sperm balls began to aggregate at the center of some follicles and many primary and secondary spermatogonial cells developed along the inner walls of the follicles.

Oogenesis

Observed oogenic activities in Donax faba from April to March are as follows:


PLATE 5. Early stage of activation in male (H.S.)

First Reproductive Cycle

(a) Activation Stage Plate (6). This stage is characterized by many stem cells at the peripheral walls of the gonadal follicles. Only very few primary oocytes were embedded in the vesicular connective tissue of the follicles. Gonadal follicles are oval in shape and mean diameter ranged between 100 µm and 135 µm.

(b) Maturation Stage Plate (7, 8). Ovaries obviously increased in size (in May) where follicular diameter reached about 250.5 µm. Presence of many large free oocytes growing at a rapid rate where diameter ranged from 25 µm to 38 µm. Many stalked oocytes were seen attached to the follicular walls protruding to the center of the follicles.

(c) Spawning Stage Plate (9). In June, the ovarian follicles were partially vacuolated. Inter-follicular spaces shrunk, mean diameter is 125 µm. Mature ova decreased in number and the follicular lumend appeared empty and translucent .

(d) Resting Stage Plate (10). In July, the follicles were elongated and compressed, have extruded all their mature ova. Most clams entered gradually the resting stage. In-tra-follicular spaces disappeared and interfollicular spaces became very thin.

The Second Reproductive Cycle

This cycle started and followed the same course of development as the previous cycle; it started in August and ended in March.

Discussion

Donax faba occurs almost everywhere along the east coast of the Red Sea and offshore islands which consist mainly of sandy beaches lying on coral platforms. These ex

64 A.A. Eshky

PLATE 6. Activation stage showing (1) formation of stem cells and (2) few primary oocytes (H.S.).

PLATE 7. Early stage of maturation in female (H.S.) showing free oocytes.


PLATE 8. Advanced stage of maturation in female (H.S.) showing stalked oocytes.

PLATE 9. Stage of partial spawning in female (T.S.) showing mature ova.

66 A.A. Eshky

PLATE 10. Resting stage with highly shrunk gonadal follicles in female (H.S.).

tend over great distances (1000 km) along the shore line of the east coast of the Red Sea interrupted only by mangrove creeks where fine grain size of sand prevents colonization by Donax faba which prefers coarser sand. Similar results were reported for the same species by Alagarswami[4] from India and Smith[3] from Tanzania. The distribution of Donax faba in the Red Sea is also restricted to the sheltered sandy beaches. The clams zone is separated from the fringing reef by the reef crest and a shallow back lagoon 16050 m in width and only 0.5-1 m in depth. The reef crest is submerged in winter but is exposed in July and August and the lagoon is sometimes reduced to a series of shallow pools. For this reason the distribution of Donax faba in the Red Sea and in the offshore islands is restricted to sheltered beaches. However, this is in conflict with the observation of Smith[3] who observed Donax faba on exposed sandy beaches of E. Africa. Al-agarswami[4] also reported the same species from exposed beaches in India. Other members of same genus were also reported from exposed beaches from different parts of world[16,42-45].

According to Smith[3], the clam maintained a feeding position within the wash zone by migrating up and down the beach tide. Wade[16] noted that population of Donax striatus inhabiting the shallow sloping beaches of Trinidad, where the water table is less than 10 cm below the sand surface, did not display tidal migration. Mclachlan et al.[43]; Prosch and Mclachlan[20]; and Theodore et al.[42] have indicated that Donax serra does not exhibit a tidal pattern of movement, like most members of this genus, but rather a semilunar migratory pattern. In the present investigation it has been noticed that Donax faba remained quiescent in the sand just below the high tide mark and that there was no


evidence to suggest either tidal nor semilunar migration for this species on the beach. This may be due to the shallow water table (< 10 cm) over the spring and neap tidal cycle where the maximum diel tidal range is < 30 cm and on beaches having a slope of about 1:15, this results in an effective intertidal habitat of approximately 90-100 cm and also may be due to the impressive digging ability of Donax faba. However, measurements of the position of Donax faba to the datum point revealed that the clams were able to maintain their position in the saturated zone at all phases. The position occupied on the saturated zone by the Donax faba population varies with the variation in sea level due to the monsoon effect.

Measurements of the positions of tagged clams every month during the period of the investigation in relation to datum point has indicated that there were clear relationship between the sea level and the position of the clams. The difference can be seen clearly between January and August were the vertical position between these two months may extend more than one meter. The response of Donax species to the tidal cycle has been described by Wade[16], Tiffany[46], and Ansell and Trueman[17] who observed that during a rising tide, the Donax are washed out or leave the sediments in response to the acoustic shock from breaking wave and liquification of the sand and are carried upshore in the wash. During the ebbing tide the Donax respond to the periodic drying of sand between wave swashes by moving to the sand surface where they are carried down shore by the backwash and burrow in the saturated sand. Cubit[47] described the tidal movements of Emerita analoga and described their movements to a similar responses to changes in the fluidity of the sand. The observed seasonal migration in Donax faba may be due to the clam population following the movements of the low water table due to seasonal variation in the sea level. Magnus[48] has reported similar behaviour for the brachyuran crab Ocypode saratan from the northern part of the Red Sea. Eshky[10]

reached the same conclusion for the fiddler crab Uca inversa from the south part of the Red Sea. This investigation is a first attempt to explain the changing distribution of the clams of the Red Sea in terms of seasonal migration rather than diel, tidal or semilunar migration as has been mentioned in the literature . In addition, it has been shown that due to the relatively shallow sloping beach, the small tidal magnitude and also due to the impressive digging ability, Donax faba can remain close to the saturated zone and therefore, reduce the need for tidal migration.

Donax faba is well known to show dramatic density changes throughout the year. A peak density in the present investigation occurred in November declining to 30/m2 in January. Alagarswami[4] reported a peak density of Donax faba from India of 217/m2 in March declining to 89/m2 in November. Smith[3] investigated the same species from the East coast of Africa and indicated a peak of density of 2729/m2 of Donax. Nayar[21]

who investigated Donax cuneatus from India a peak density of 472/m2 in June declining to 185/m2 in August.

The analysis of growth rate in Donax faba in the present investigation demonstrated different seasonal patterns of growth. The greatest increase in the growth rate took place in the summer. Similar results were reported for the same species by Alagarswami[4]

and Smith[3] and also for other Donax species from different parts of world[21-24,49]

68 A.A. Eshky

Hibish and Koehn[50] have related the increase in growth rates of soft tissue during summer coincident with maximal rates of energy gained. Eshky and Ba-Akdah[7] have shown that high temperature affects both the oxygen consumption and the heart rate of Donax faba. Also Mori et al[27] has indicated a similar effect of high temperature on the metabolism of the commercial Oyster Crassostrea gigas.

Spawning activity appears to affect growth rate. Quayle[25] and Auger[26] observed slightly lower rates of shell growth in oysters during August than July when spawning activity peaked at temperatures reaching 20ºC. Suppression of energy reserves or their diversion from growth to reproductive activity seems likely to be the reason[27]. Poor winter growth in the present study could be due to the same effect where slow winter growth rate coincided with spawning activity of the clams.

Donax faba has a prolonged breeding period of two different peaks of spawning. The small peak took place in June and the large one in November and December. Al-agarswami[4] has observed that Donax faba from the Mandapam coast of India has only one spawning peak which occurred in May and June and he indicated that the major determinants of spawning time are water temperature and salinity. Rao[30] observed one single distinctive annual reproductive cycle of Donax cuneatus which took place between September and December and he related this reproductive activity to low temperature and salinity. Nayar[21] observed one reproductive cycle for D. cuneatus where spawning commenced in January and ceased in April when the water temperature increased.

These two reproductive cycles of D. faba in the present study corresponded with the phytoplankton peak which occurred at same period[51]. Therefore, one possible reason for increased reproductive activity in the pre and post monsoon periods could be the availability of food for the clams larvae. The same explanation was forwarded by Boolootian et al.[31] and Siddiqui and Ahmed[35] who reached the same conclusion: that the pre and post monsoon periods are relatively calm periods during which lesser wastage of eggs can be expected. Similar conclusion was also reached by Phillay and Nair[33]

while studying the breeding biology of the crabs from the south west of India. According to them, the availability of food for the young ones during the planktotrophic life is a very important factor controlling the breeding season. Goodbody[32] has suggested that there may be some relationship between breeding periods and the presence of a particular fraction of species in the plankton at a certain season of the year. Borrero[34]

investigated the relationship between tidal height and reproductive variation among the population of Geukensia demissa from South Carolina. He also made a comparison of the productive cycles of populations of G. demissa from different latitudes on the east coast of the United States and found that the microgeographic variation in the timing of reproductive activity may be as great as the latitudinal. The level of occurrence in the intertidal zone, and hence length of submersion and potential feeding time exert a profound influence on the timing of the reproductive cycle of G. demissa. Newell, et al.[28]

observed that differences in food quantity and/or quality and not temperature were the major determinants of the timing of gameto-genesis and spawning of the Mytilus edulis population from the east coast of the United States. The present study supports the above conclusions. However, it is of interest to note that some marine brachyuran crabs,


Metapograpsus messor, Ocypode saratan and Grapsus tenuicrustatus breed continuously throughout the year and spawning peaks around the time as Donax faba. It is likely that there is a strong relationship between breeding periods, not only for Donax faba but also for most of the marine invertebrate in the Red Sea, and the availability of food during the monsoon effect.

References

[1] McIntyre, A.D., The meiofuna and macrofauna of some tropical beaches. J. Zool. Lond., 156: 377-392 (1968).

[2] Trevallion, A., Ansell, A.D., Sivadas, P. and Narayanan, B., A preliminary account fo two sandy beaches in south west India. Mar. Biol., 6: 268-279 (1970).

[3] Smith, D.A.S., Polymorphism and selective predation in Donax faba (Gmelin). J. Exp. Mar. Biol. Eco., 17: 205-219 (1975).

[4] Alagarswami, K., Studies on some aspects of biology of the wedge clam Donax faba (Gmelin) from Mandapam coast in the Gulf of Mannar, J. Mar. Biol. Ass. India, 8(1): 56-76 (1966).

[5] Morley, N.J.F., The coastal waters of the Red Sea. Bull. Mar. Res. Centre, Saudi Arabia, 5: 1-19 (1975).

[6] Eshky, A.A., Aspects of the ecology behavior and physiology of the ghost crab Ocypode saratan (Forskal), Ph.D. Thesis, University of Glasgow: 250 (1985).

[7] Eshky, A.A. and Ba’Akdhah, M.A., Effects of temperature on the oxygen consumption and heart rate in the intertidal wedge clam Donax faba (Gmelin), JKAU Mar. Sci., 13: 81-90 (1992).

[8] Eshky, A.A., Atkinson, R.J.A. and Taylor, AC., Physiological ecology of crabs from Saudi mangrove. Mar. Ecol. Prog. Ser., 126: 83-95 (1995).

[9] Hodgkin, E.P., Catastrophic destruction of the littoral fauna and flora near Fremantle. West Aust. Nat., 7: 6-11 (1959).

[10] Eshky, A.A., Bahavioural ecology and heart responses of the mangrove crabs (Uca-spp) at Madia Creek Jizan city, JKAU Mar. Sci., 3: 67-79 (1992).

[11] Morcos, S.A., Physical and chemical oceanography of the Red Sea. Oceanogr. Mar. Biol. Ann. Rev., 8: 73-202 (1970).

[12] Patzert, W.C., Wind-induced reversal in Red Sea circulation. Deep Sea Res., 21: 109-121 (1974). [13] Patzert, W.C., Seasonal variations in structure and circulation in the Red Sea. Hawaii Institute of Geo

physics, University of Hawaii. Report HIG-72-13 Xvii + 58 p. (1972). [14] Loesch, H.C., Studies on the ecology of two species of Donax on Mustang Islands, Texas. Publications

of the Institute of Marine Science of the University of Texas, 4: 201-227 (1975). [15] Turner Jr., H.J. and Belding, D.L., The tidal migrations of Donax variabilis Say. Limnol. Oceanogr, 2:

120-124 (1957). [16] Wade, B.A., Studies on the biology of the West Indian beach clam Donax denticulatus Linne. 1. Ecol

ogy, Bull. Mar. Sci., 17: 194-174 (1967). [17] Ansell, A.D. and E.R. Trueman, The energy cost of migration of the bivalve Donax on tropical sandy

beaches. Mar. Behav. Physio., 2: 21-32 (1973). [18] Leber, K.M., Bivalves (Tellinacea: Donacidae on a North Carolina beach: contrasting population size

structures tidal migrations. Mar. Ecol. Prog. Ser., 7: 297-301 (1982). [19] Ansell, A.D., The biology of the genus Donas. In: Sandy beaches as ecosystems, edited by A. McLach

lan and T. Erasmus, Junk Publ., The Hague, pp. 607-636 (1983). [20] Prosch, R.M. and Mclachlan, A., The regeneration of suf- zone nutrients by the sand mussel, Donax

serra Roding. J. Exp. Mar. Biol. Ecol., 90: 221-233 (1984). [21] Nayar, K.N., Studies on the growth of wedge clam, Donax (Latona) Cuneatus (Linnaeus). Indian J.

Fish., 2: 325-348 (1955). [22] Coe, W.R., Ecology of the bean clam, Donax gouldi on the coast of Southern California, Ecology, 36:

512-515 (1955). [23] Ansell, A.D., Distribution growth and seasonal changes in biochemical composition for the bivalve Do

nax vittatus (De Costa) from Kames Bay, Millport, J. Exp. Mar. Biol. Ecol., 10(2): 151-160.

70 A.A. Eshky

[24] Devilliers, G., Growth, population dynamics, a mass mortality and arrangement of white sand mussels, Donax serra (Roding) on beaches in the Southwestern Cape Province, Investl. Rep. Sea Fish. Brch., S. Afr., 109: 1-31 (1975).

[25] Quayle, D.B., Pacific oyster culture in British Columbia. Bull. Fish. Res. Bd Can. 169, 1-192. Summer, C.E. (1974). Oysters and Tasmania. Part 2. Tasmanian Fish. Res., 8(2): 1-12 (1969).

[26] Auger, C., Etude de deux vairietes de Crasso-strea gigas Thunberg leu acclimation on riviere d’Etel (Morbihan). Ph.D. Thesis, University of Paris (1976).

[27] Mori, K., Toyoshima, K. and Usuki, I., Studies on the mass mortality of the oyster in Matsushima Bay. IV. Changes in the physiological activity and the glycogern content of the oyster during the stages ofsexual maturation and spawning. Bull. Tohoku Reg. Fish. Res. Lab., 25: 49-63 (1965).

[28] Newell, R.I.E., Hilbish, T.J., Koehn, R.K. and Newell, C.J., Temporal variation in the reproductive cycle of Mytilus edulis L. (Bivalvia Mytilidae) from locations on the east coast of the United States. Biol. Bull. 162: 299-310 (1982).

[29] Bayne, B.L. and Newell, R.C., Physiological energetics of marine molluscs. In: The Mollusca, Vol. 4, part 1, pp. 407-415. Ed. by A.S.M. Saleuddin and K.M. Wilbur. New York: Academic Press (1983).

[30] Rao, K.A., Annual reproductive cycle of the wedge clam Donax cuneatus (Linnaeus). J. Mar. Biol. Assoc. India, 9(1): 141-146.

[31] Boolootian, R.A., Giese, A.C., Faraian, A.F. and Tucker, J., Reproductive cycles of five west coast crabs. Physiol. Zool., 32: 213-220.

[32] Goodbody, I.M., Breeding seasons in tropical marine invertebrates. Proc. Ass. Isl. Mar. Lab., 4th meeting (abs) 8-9 (1962).

[33] Pillay, K.K. and Nair, N.B., Observations of the breeding biology of some crabs from the south west coast of India. J. Mar. Biol. Assoc. India, 15: 754-770 (1973).

[34] Borrero, F.I., Tidal height and gametogenesis: reproductive variation among populations of Geukensia, Vol. 173-168 (1987).

[35] Siddiqui, G. and Ahmed, M., Distribution and abundance of marine brachyuran crabs on two exposed rocky ledges near Karachi (Pakistan, Arabian Sea). Pakistan J. Zool., 23: 57-63 (1991).

[36] Folk, R.L., Petrology and sedimentary rocks. Austin, Texas: Hemphill Publishing Co., 182 p. (1974). [37] Gray, J.S., The ecology of marine sediments. Cambridge: Cambridge University Press, 185 p. (1981). [38] Koenig, P., General circulation model of the Red Sea. Technical Report No. 38 presented by Prevssag

Marine Technology Dept. to Saudi-Sudanese Commision for the Exploitation of the Red Sea Resources. Hamburg: Institute of Oceanography, University of Hamburg, 53 p. (1982).

[39] Winber, G.G., Methods of the estimation of production of aquatic animals. Academic Press. London and New York: 1-175 (1971).

[40] Shaw, W.N., Seasonal gonadal changes in female soft-shell clam, Myva arenaria, in the Tred Arm Rivers, Maryland. Proc. Nat. Shell Fish. Ass., 53: 120-132 (1964).

[41] Shaw, W.N., Seasonal gonadal cycle of the soft shell clam Mya arenaria in Maryland, U.S. Fish and Wildlife Serv. Spec. Fish, 508: 1-5 (1965).

[42] Theodore, E.D., Clark, D.J., McLachlan, A. and Toit, P. , Distribution and abundance of Donax serra Roding (Bivalvia: Donacidae) as related to beach morphology. I. Semilunar migrations. J. Exp. Mar. Biol. Ecol., 102: 121-131 (1986).

[43] McLachlan, A., Hanekom, N., Aspects of the biology, ecology and seasonal fluctuations in biochemical composition of Donax serra in the East Cape. Soc. S. Afr. J. Zool., 14(4): 183-193 (1979).

[44] Bonsdorff, E. and Nelson, W.G. (1992) The Ecology of coquina clams Donax variables Say. 1822 and Donax parvula Philippi, 1849 on the east coast of Florida. Veliger, 35: 358-365 (1992).

[45] Neuberger, L., Achituv, Y. and Mizrani, L., The ecology of Donax Linnaeus and Donax semistriatus Poli from Israel. J. Exp. Mar. Biol. Ecol., 134(3): 203-220 (1990).

[46] Tiffani III, W.J., The tidal migration of Donax variabilis Say (Mollusca: Bivalvia). Veliger, 14: 82-85 (1972).

[47] Cubit, J., Behavior and physical factors causing migration and aggregation of the sand crab Emerita analoga (Simposon). Ecology, 50: 118-123.

[48] Magnus, D., Zur Okologie des Landerinsiedlers Coenobita jousseaumei Bouvier und der krabbe Ocypode aegyptiaca Gerstaecker am Roten Meer. Verh. dt. Zool. Ges., Bonn, 316-329 (1960).


[49] Smith, D.A.S., Polymorphism and population density in Donax rugosus L. (Lamellibranchiata: Donacideae). J. Zool. Lond., 164: 429-441 (1971).

[50] Hilbish, T.J. and Koehn, R.K., Physiological basis of natural selection at the Lap locus. Evolution, 39: 1302-1317 (1985).

[51] Shaikh, E.A. and Dowidar, J.C., Phytoplankton ecology and production in the Red Sea off Jeddah, Saudi Arabia. Marine Biology, 92: 405-416 (1986).

72 A.A. Eshky

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