Journal of the Persian Gulf (Marine Science)/Vol. 3/No. 9/September 2012/10/33-42

The Gastropod Fauna along the Bushehr Province Intertidal Zone of the Persian Gulf

Kohan, Ahmadreza*; Badbardast, Zahra; Shokri, Mohammadreza

Faculty of Biological Science, Shahid Beheshti University, Tehran, IR Iran

Received: April 2012 Accepted: July 2012

© 2012 Journal of the Persian Gulf. All rights reserved.

Abstract The gastropod fauna of Bushehr Province intertidal zone at the Persian Gulf were identified following an investigation starting spring 2009 until winter 2011. Bushehr coastline is a 673.62 km stretch along the northern and northeastern coast of the Persian Gulf. Sampling took place from Deylam at Bushehr-Khuzestan borderlines, extending southeastward through Genaveh, Bushehr, Bolkheyr, Kabgan, Dayer and Nayband at Bushehr-Hormozgan provincial borderlines. A total of 87 gastropod from 54 families were identified. The most frequent family with 7 spp. was , followed by Strombidae (4 spp.), , Potamididae, Olividae and Epitoniidae (3 spp. each).The most frequent species was Planaxis sulcatus observed in all 7 stations, followed by Turitella fultoni, mutabilis and Thais savignyi occurring in 6 stations. The Jaccard Similarity measure showed the highest similarity for Genaveh and Bushehr (0.818) and the lowest similarity for Genaveh and Deylam (0.152).This study provided the first comprehensive list of species occurring in Bushehr Province intertidal zones yet.

Keywords: Gastropoda fauna, Intertidal zone, Distribution, Bushehr, Persian Gulf

1. Introduction habitats ranging from the deepest ocean basins to the supra-littoral. The class Gastropoda, large taxonomic class Marine gastropod species of the Persian Gulf are within the phylum , consists of and highly varied and abundant forming an important slugs (Bouchet et al., 2005). The class contains source of food for higher consumers (Al-Khayat, second largest number of species after the insects 2008). Gastropods are also important contributors to (Abbott, 2001) majority of which live in the marine coastal food chains, especially in mangrove forests ecosystems with a wide range of habitats. They occupy (Morrisey et al., 2003), to human uses, as food, e.g. all marine habitats ranging from the deepest ocean Turbo spp. and Strombus spp. (Sundaram, 1974) or basins to the supra-littoral. Environmental and medical utilities, e.g. Conus spp. (Olivera and biological factors, such as that of the Persian Gulf, Teichert, 2007). In addition, immigrant birds are profoundly influence the occurrence and distribution of attracted to Gastropod species in coastal areas (Bond marine invertebrates in general, and marine gastropods and Diamond, 2007). in particular. As such, gastropods, occupy all marine The Persian Gulf biota have been subject of study * E-mail: [email protected] by many scientists. Early studies were conducted in 33

Kohan et al. /The Gastropod Fauna along the Bushehr Province Intertiddaal Zone of the Persian Gulf early 1900 by Standen (1901) and Melvill (1928). A collect gastropods in mudddy shores, first five comprehensive survey was carried out by Danish centimeters of sediments (aeerobic zone) were picked Scientific team headed by Belgvad et al. (1937- and separated using a system of sieves of different 1938), whom published the results in a book entitled, mesh sizes (10 mm, 1 mmm and 0.5 mm). To find “Danish Scientific Investigation in Iran” during 1944 burrower species in sandy shores, sands were dug to and 1949. Other scientific studies include, the a depth of about 20 centimetters in several points. In German Oceanographic Vessel “Meteor” (19665) rocky shores, all aspects of rocks and boulders were survey findings, Biggs and Grantier (1960), Basson investigated (Figures 2 and 3). et al. (1977) and Sharabati (1981). More recent All gastropod speciemen were washed and studies have mainly concerned molluscs, for preserved in 70% Ethyl alcohol and 4% formalin. example, studies of Tajalipour (1970-1974), Al- Khayat (1977, 2005, 2006, 2008), Hasan (1996, All gastropod species were identified according to 1974), Rezai et al. (1995), Vazirizadeh and Arebi the lowest reliable taxonomic level. The following (2010), Ghasemi et al. (2011). systematic references were used as important guides Although, Bushehr coastline offers a unique for the identification of tthe species concerned: opportunity to study differences between different types Hoseinzahdeh Sahafi (2006), Taylor and Sohl of intertidal substrates, primarily because of coastal (1962), Angeletti (1978), OOpresko et al. (1976), diversity, there is very little information on the Bushehr Bouchet and Rocroi (2005)), Tunnell et al. (2010), Province intertidal gastropods population. Hence, tthhe Abbott et al. (2001) and Abbott and Morris (2001). present work was carried out to determine the intertidal gastropods population distribution of this zone.

2. Material and Methods

2.1. Study Area

The present study was conducted in Bushehr Province coastlline (27°.27’ N to 30°.26’ N and 50°.93’ E to 52°.37’ E), encompassing the northern and northeastern cooast of the Persian Gulf (Figure1). Bushehr Province coastline is 673.62 km long and 35- 765 m wide (Sharifipour et al., 2006). Sampling was Fig. 1: Location of the study area, Bushehr Province coasts, the carried out from Deylam at Bushehr-Khuzesttaan Persian Gulf borderlines, extending southeastward through Genaveh, Bushehr, Bolkheyr, Kabgan, Dayer and Nayband, at Table 1. Sampling stations of investtigated area Geographic No. Station Substrate Bushehr-Hormozgan borderlines (Table 1). Coordinates 1 Deylam 50°.93’ E , 30°.26’ N Muddy, Sandy 2 Genaveh 50°. 49’ E , 29°.33’ N Sandy, Rocky 2.2. Sampling 3 Bushehr 50°. 50’ E , 28°.54’ N Sandy, Rocky 4 Bolkheyr 51°. 55’ E , 28°.32’ N Sandy The gastropod fauna of the Bushehr Provinnce 5 Kabgan 51°. 17’ E , 28°.12’ N Sandy intertidal zone of the Persian Gulf were sampled by 6 Dayyer 51°. 56’ E , 27°.49’ N Rocky, Sandy, Muddy Sandy, Muddy (mangrove 7 Nayband 52°. 37’ E , 27°.27’ N handpicking during spring, 2009 and winter 2011. To forest), Rocky

34 Journal of the Persian Gulf (Marine Science)/Vol .3/No .9/September 2012/10/33-42

Table 2. Existence ranges of gaasstropod species 0 - 20 - D (%) 40 - 59.99 60 - 79.99 80 - 100 19.99 39.99 Very Relatively Common Very Rarity Rare sp. rare sp. common sp. sp. common sp. Given this (Table 2) a very rare species is which exists in 0 – 19.99% of Bushehr Province coastline. The Jaccard Similarity coefficient was used to determine similarity betwweeen stations.

Fig. 2: Rocks and boulders in rocky shores of Dayyer Station 3. Results

A total of 87 species from 54 families were identified in 7 stations (Table 3, Plates 1, 2 and 3). Thirty-seven species occurred only in one station. For example, Acteocina involuuta was found only in Dayyer and Atys cylindricus only in the Nayband area. The family Trochidae was the most frequent family (7 spp.), followed by Strombidaee (4 spp.), Pyramidellidae, Potamididae, Olividae and Epitoniidae (3 spp. each). The most frequent species was Planaxis sulcatus (in 7 stations) followed by Turitella fultoni, Thais mutabilis and Thais saviiggnyi (in 6 stations) (Plates 1, 2, 3). The identified gastropod species were categorized to very rare and very common species based on their distribution ranges (not their frequencies).The histogram of distribution rrange demonstrated that the most and the least numbers of Bushehr Province Intertidal gastropods are categorized in very rare species and very common species divisions, Fig. 3: The shells of the dead specimens of Cerithidea cingulata (left) covered the entire substrate in Bushehr station and respectively (Figure 4). This meant that the identified Onchidium peronii, an air breathing gastropod species from species predominantly were restricted to small areas. Dayyer intertidal zones Very rare species occurred in as much as 19.99% of Bushehr Province coasttline, perhaps because of 2.3. Data Analysis various conditions in different parts of Bushehr coastline. To determine distribution ranges (D) of Gastropoda Results of the Jaccard Similarity Coefficient were species, Equation 1 was used. In this formula: “n” is used to draw the linkage dendrogram (Figure 5). the number of stations in which a specific species Gastropod species could be grouped into four zones: was present and “N” is the number of all investigated Zone 1 included Bushehr and Genaveh, Zone 2 stations. included Dayyer, Deylam and Bolkheyr, Zone 3 100 (1) included Kabgan and Zone 4 included Nayband. 35 Kohan et al. /The Gastropod Fauna along the Bushehr Province Intertidal Zone of the Persian Gulf

Table 3-1. The identified gastropod species of intertidal zone of Bushehr Province in sampling stations Species Deylam Genaveh Bushehr Bolkheyr Kabgan Dayyer Nayband Acmaea profunda - + + + - + + Acme polita + - - - + - - Acteocina involuta* - - - - - + - Anachis misera - + + - - - - Ancilla castanea* - - - - + - - Architectonica perspectiva - + + - + - + Atys cylindricus* ------+ Babylonia spirata - - - + - + - Balcis alba * - - - - + - - Bufonaria echinata + + + - + - + Bulla ampulla - + + - - - - Caecum gracile + - - - - + + Cellana karachiensis - + + - - - - Calyptraea edgariana + - - - - + + Cassidula labrella* ------+ Cerithidea cingulata + + + - - + + cerithium* ------+ Cerithium columna + - - - + + + Citharmagglia sp.* ------+ Clypeomorus bifasciatus + - - - - + + Conus flavidus* - - - - + - - Conus quercinus* - - - - - + - Crassispira flavidulus* - - - - + - - Cyclostrema crinium* ------+ Cyclostrema sprenum - - - - - + + Cymatium aquatile - + + - - - - Cypraea annulus + - - - - - + Diodora bombayana + - - - - - + Diodora funiculate + - - - - - + Epitonium angulatum + - - - - - + Epitonium pallasii + - - - + + - Epitonium sp.* ------+ Ethalia sp.* ------+ Euchelus asper - + + - + - - Finella sp.* - - - - - + - Gibbula declivis* - - - - + - - Granulina sp.* - - - - - + - Haminea vitrea* - - - - + - - Hydrobia sp.* - - - - - + - Iravadia densilabrum* ------+ Iravadia quadrasi* ------+ Littorina intermedia* ------+ Melanella cumingii + - - - - + + Mitrella blanda - + + - - - + Mitrella misera - + + - - + - scolopax - + + - - - - Nassariusarcularius plicatus + - + + - + - Nassarius deshayesiana - + + - - - - vitellus* - - - - - + - Nerita melanotragus - + + - - - - Nerita textilis - + + - + - - didyma - + + + - + + Niso venosa + - - + + + + bulbosa - + + - + - - Oliva oliva + - + + - + - Onchidium peronii - - + - - + - * - - - - + - - Phasianella solida* - - - - - + - Planaxis sulcatus + + + + + + + nedyma* ------+ Pupa affinis* - - + - - - - Scaphander sp.* ------+ Seila bandorensis* ------+

36 Journal of the Persian Gulf (Marine Science)/Vol .3/No .9/September 2012/10/33-42

Table 3-2. The identified gastropod species of intertidal zone of Bushehr Province in sampling stations

Species Deylam Genaveh Bushehr Bolkheyr Kabgan Dayyer Nayband Sipphonaria denticulata - + + - + - - Stenothyra sp.* ------+ Stosicia annulata* ------+ Strombus decorus persicus - + + - + + + Strombus mutabilis* - - - - - + - Strombus plicatus sibbaldi* - - - - - + - Telescopium telescopium + - - - + + + Terebralia palustris* ------+ Thais mutabilis - + + ++ + + Thais savignyi - + + ++ + + Tibia insulaechorab curta + - - - - - + Terebra sp.* ------+ Tricchotropis sp.* ------+ Triphora perversa + + + - - + + Trochus erythraeus + + + - - + + Trochus radiatus - + + - - - - Truncatella subcylindrica - - - - - + + Turbo coronatus - + - + + + + Turbo radiatus - + - - + - - Turbonilla linjaica + - - + - + + Turritella fultoni + + + + - + + Turitella sp.* ------+ Umbonium sp.* - - - - - + - Umbonium vestiarium + + + - - + +

Total Species Number 24 29 31 12 24 38 49 * : Species occurring in only one station

Fig. 4: Abundance of very rare to very common species of Bushehr Province coastal area Fig. 5: The linkage between difffferent stations

37 Kohan et al. /The Gastropod Fauna along the Bushehr Province Intertidal Zone of the Persian Gulf

4. Discussion tolerance and thus adapt efficiently to fluctuating environmental factors. Only 5 % of Bushehr Province Considering the results of this study and other intertidal gastropods were distributed in more than 80% researches in the Persian Gulf region, the high of coastline (Figure 4). gastropod diversity was expected. Al-Khayat (1977) Planaxis sulcatus was reported by Al-Khayat (1997) reported 99 gastropod species of Qatari waters of the as dominant gastropod species in the Qatari coasts of Persian Gulf. Greater species abundance in that study the Persian Gulf. This species with its adaptations to compared with the present study, could be mostly live in different environmental conditions, occupied due to more extensive sampling areas including approximately the entire Persian Gulf coastlines. upper areas of sub-littoral zone. Hasan (1996) Studies covering gastropod communities in intertidal identified 62 gastropod species in intertidal zone of zones are few, not only in the Bushehr Province, but Saudi Arabian coasts of the Persian Gulf. Less also, in the entire Iranian coasts of the Persian Gulf and habitat diversity and shorter sampling period could the Oman Sea (Ghasemi et al., 2011). Although, be the reasons of the less number of identified identifying list of gastropod species of Intertidal zone of species in Saudi Arabian coasts. Bushehr Province were conducted and results presented The eastern Bushehr Province coasts recorded the in this study, more frequent and comprehensive highest gastropod species numbers. The high investigations along the entire northern coastlines of the diversity in habitats might be the main reason. These Persian Gulf and the Oman Sea are needed. parts possess the most habitat diversity which included muddy flats, sandy and rocky shores and References mangrove forests (Table 1). Some parameters which have significant impacts on benthic Abbott, R. T. and Morris, A. P., 2001. A Field Guide communities include sediments particle size (Basson to Shells: Atlantic and Gulf Coasts and the West et al., 1994), salinity (Coles and Mc Cain, 1990), Indies. Houghton Mifflin Harcourt. 512 P. water currents (Shappard, 1992) and pollutants Abbott, R. T., Zim, H. S. and Sandstrom, G. F., (Coles and Mc Cain, 1990). 2001. Seashells of North America: A Guide to The Jaccard Similarity measure demonstrated the Field Identification. St. Martin's Press. 280 P. highest and the lowest similarity for Genaveh and Al-Khayat J. A., 2005. Some macrobenthic Bushehr (0.818) and Genaveh and Deylam (0.152), invertebrates in Qatari waters. Qatar University respectively (Figure 5). This could be attributed to Science Journal, 25 (1): 126-136. remarkable similarity in substrates of Genaveh and Al-Khayat, J. A. and AL-Mohannadi M.S., 2006. Bushehr and noticeable difference in substrates of Ecology and biology of the benthic bivalve Genaveh and Deylam (Table 1). Nayband and Kabgan Aminatis umbonella (Lamark) in Khor Al-Adaid, showed relatively exclusive species composition, Qatar. Egyptian Journal of Aquatic Research, 32 thereby highlighting their higher conservation value. (1): 419-430. The highest abundance of very rare species (43%) Al-Khayat, J. A., 1997. The marine mollusc of the in comparison with other divisions (Table 2 and Figure Qatari water. Qatar university Science Journal, 17 4) could be because of differences in substrate quality (2): 479-491. (Sharifipour et al., 2006) and other environmental and Al-Khayat, J. A., 2008. Molluscs of the state of biological characteristics of intertidal zones influencing Qatar. Qatar Biodiversity Newsletter, 2 (1). 1-5. distribution of gastropod species along entire coastline. Angeletti, S., 1978. The Seas and their Shells, a Collector Given this, gastropods are forced to develop higher Guide to the Seashells of the World. Doubleday and

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Company. Garden City, New York. 303 P. different ages in New Zealand. Estuarine, Coastal Basson, P. W., Buchard, J. E., Hardy, J. T. and Price, and Shelf Science, 56(3-4): 581-592. A. A. G., 1977. Biotopes of the Western Persian Olivera, B.M. and Teichert, R.W. 2007. Diversity of the Gulf, Marine life and Environment of Saudi neurotoxic Conus peptides: a model for concerted Arabia. Department of Loss Prevention and pharmacological discovery. Molecular Interventions, Environmental Affairs, ARAMCO-Dhahrn, 284 P. 7 (5): 251–60. Biggs, H. E. J. and Grantier, I., 1960. A preliminary Opresko, L.,Thomas, R., Bayer, F. M. and Voss, G. list of mollusca of ras Tanura. Persian Gulf. L., 1976. Guide to the Larger Marine Gastropods Journal of Conchology. 24(11): 387-392. of Florida, the Gulf of Mexico, and the Caribbean Bond, A. and Diamond, A., 2007. Abandoned seabird Region. Miami, Fla.: University of Miami Sea eggs as a calcium source for terrestrial gastropods. Grant Program. 54 P. Canadian Field-Naturalist, 121(4): 433-435. Rezai, H., Rameshi, H. and Ranai-Rad, E. 1995. Bouchet P., Rocroi J. P., Frýda, J., Hausdorf, B., Distribution of benthic molluscs in shallow Ponder W., Valdes A. and Warén A., 2005. waters around some Iranian Islands in the Persian Classification and Nomenclature of Gastropod Gulf. Iranian Fisheries Research and Training Families. Malacologia: International Journal of Organization, Ministry of Agriculture, 168 P. (In Persian) Malacology, 47(1-2). ConchBooks: Hackenheim, Shappard, R. C. and Price, A., 1992. Marine Ecology Germany. 397 P. of the Arabian Region, Patterns and Processes in Coles, S. L., and McCain, J. C., 1990. Environmental Extremes Tropical. Academic Press. 359 P. factors effecting benthic in faunal communities of Sharifipour, R., Danehkar, A. and Nouri, J., 2006. western Persian Gulf. Marin Environmental Determination of ecological susceptibility of the Research. 29: 289-315. Bushehr Province shoreline in the northern Persian Ghasemi, S., Zakaria, M. and Mola Hoveizeh, N., Gulf. Journal of Environmental Science. 7 (1): 45-52. 2011. Abundance of molluscs (Gastropods) at Sundaram, K. S., 1974. IV Edible Gastropods. In: mangrove forests of Iran. Journal of American CMFRI Bulletin No.25, the Commercial Molluscs Science. 7(1): 660-669. of India. Nair, R V and Rao, K Satyanarayana, Hasan K. A., 1996. A taxonomic review of the (eds.) CMFRI, Mandapam Camp, pp 54-62. bivalve and gastropod mollusc fauna along the Tajalipour M., 1994. Systematic Study and Saudi intertidal zone of the Persian Gulf .Journal Distribution of Molluscs of Iranian Coasts of the of King Abdullah University: Marine Science. 7 Persian Gulf. Kheybar Publication, Tehran, Iran. (4): 245·253. 170 P. (In Persian) Hasan, A. K., 1974. Studies on Bottom Mollusca Taylor, D. and Sohl, N. F., 1962. An outline of (Gastropods and Bivalves) In Abu-Qir Bay. gastropod classification. Malacologia, 1 (1): 7-32. Alexanderia M.Sc Thesis Alexanderia University. Tunnell, J. W., Andrews, J., Barrera, N. C. and 116 P. Moretzsohn, F., 2010. Encyclopedia of Texas Hoseinzadeh Sahafi H., 2006. Atlas of Persian Gulf Seashells: Identification, Ecology, Distribution, and Oman Sea Molluscs. Iran Fishery Research and History. Texas A&M University Press, Organization Publication, Tehran, Iran. 248 P. (In Texas, USA. 512 P. Persian) Vazirzadeh, A. and Arebi, I., 2011. Study of Morrisey, D., Skilleter, G., Ellis, J., Burns, B., macrofaunal communities as indicators of sewage Kemp, C. and Burt, K., 2003. Differences in pollution in intertidal ecosystems: A case study in benthic fauna and sediment among mangrove bushehr (Iran). World Journal of Fish and Marine (Avicennia marina var. australasica) stands of Sciences 3 (2): 174-182.

39 Kohan et al. /The Gastropod Fauna along the Bushehr Province Intertiddaal Zone of the Persian Gulf

Plate 1. The images of identified gastropod species along Bushehr Province coastline in different iinvestigated stations

2 1 3 4 5

6 7 8 9 10

15 12 11 13 14

19 16 17 18 20

21 22 23 24 25

29 26 27 30 28

1.Acmaea profunda 2.Acme polita 3.Acteocina involuta 7.Babylonia spirata 8.Balcis alba 9.Ancilla casttanea 13.Cassidula labrella 14.Cellana karachiensis 15.Cerithidea cingulata 19.Clypeomorus bifasciatus 20.Conus flavid 21.Conus quercinus 25.Cypraea annulus 26.Diodora funiculate 27.Epitoniumm pallasii

40 Journal of the Persian Gulf (Marine Science)/Vol .3/No .9/September 2012/10/33-42

Plate 2. The images of identified gastropod speciees along Bushehr Province coastline in differrent investigated stations

1 2 3 4 5

7 8 9 6 10

12 15 11 14 13

20 16 17 18 19

21 22 23 24 25

26 27 28 29 30

1.Gibbula declivis 2.Granulina sp 3.Haminea vitrea 4.Hydrrobia sp. 5.Iravadia densilabrum 6.Iravadia quadrasi 7.Littorina intermedia 8.Melaanella cumingii 9.Mitrella blanda 10.Mitrella misera 11.Murex scolopax 12.Nassssariusarcularius plicatus 13.Nassarius deshayesiana 14.Naassarius deshayesiana 15.Natica vitellus 16.Nerriita melanotragus 17.Nerita textilis 18.Neverita didyma 19.Niso venosa 20.Oliva bulbosa 21.Oliva olive 22.Onchidium peroniii 23.Otopleura mitralis 24.Phasianella solida 25.Planaxis sulcatus 26. 27.Pupa affinis 28.Scaphander sp. 29.Seila bandorensis 30.Siphonaria denticulata

41 Kohan et al. /The Gastropod Fauna along the Bushehr Province Intertiddaal Zone of the Persian Gulf

Plate 3. The images of identified gastropod species along Bushehr Province coastline in different iinvestigated stations

2 3 4 1 5

8 6 7 9 10

14 12 13 11 15

19 16 17 18 20

21 24 25 22 23

26 27

1.Stenothyrra sp. 2.Stosicia annulata 3.Strombus mutabilis 4.Strroombus plicatus sibbaldi 5.Strombus decorus persicus 6.Telescopium telescopium 7.Terebra sp. 8.Terrebralia palustris 9.Thais mutabilis 10.Thais savignyi 11.Tibia insulaechorab curta 12.TTeerebralia palustris 13.Trichotrropis sp. 14.Triphora perversa 15.Trochus erythraeus 16.TTrrochus radiates 17.Truncatella subcylindrica 18.Turbo coronatus 19.Turbo radiatus 20.TTuurbonilla linjaica 21.Turritella fultoni 22.Umbonium vestiarium 23.Diodora bombayana 24.CCyyclostrema sprenum 25.Epitonium sp. 26.Epitonium angulatuum 27.Umbonium sp.

Koohan et al. /The Gastropod Fauna along the Bushehr Province Intertidal Zone of the Persian Gulf Journal of the Persian Gulf (Marine Science)/Vol .3/No .9/September 2012/10/33-42 Journal of the Persian Gulf (Marine Science)/Vol. 3/No. 9/September 2012/10/33-42

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