Distribution of Molluscs in the Eastern Persian Gulf, PG-GOOS Cruise

Journal of the Persian Gulf (Marine Science)/Vol. 5/No. 17/September 2014/ 11 / 37-48

Amini Yekta, Fatemeh*; Jalili, Mahshid; Pourjomeh, Fatemeh Hakim Elahi, Maryam; Rezaei, Hamid

Iranian National Institute for Oceanography and Atmospheric Science (INIOAS), IR Iran.

Received: February 2014 Accepted: July 2014

Abstract Distribution of molluscs in the eastern part of the Persian Gulf were studied during the PG-GOOS cruise (Oct-Nov 2012), using the 250 cm2 Van Veen grab for sampling. Sixty gastropod and 23 bivalve taxa in addition to one scaphopod taxon were identified. Gastropods constituted 80% of molluscs. The abundance of molluscs averaged 1398.36 (±261.95) ind./m2. Costellaria sp. was the most abundant gastropod and Ervilia scaliola, the most abundant bivalve species. Abundance of molluscs in different stations showed significant differences (p<0.05). Station C, located near Abu Musa Island, with an average abundance of 8040 (±1625.30) ind./m2, was the most abundant site. Average values for Shanon and Simpson indices were 2.08 (±0.11) and 0.81 (±0.02), respectively. The average abundance of molluscs was significantly correlated with depth, sediment temperature (p<0.01), salinity and TOM (p<0.05). Mollusc diversity showed significant correlation with sediment temperature, salinity, depth (p<0.05) and TOM (p<0.01).

Keywords: PG-GOOS cruise, Mollusca, Persian Gulf, Distribution, Diversity

1. Introduction its young age (Sheppard et al., 2010). Mollusca with almost 100,000 species constitute The Persian Gulf is a shallow semi-enclosed basin the second largest animal phylum (Barnes et al., connected to the Gulf of Oman through the Strait of 2009). Many mollusc species are used as bio- Hormuz. The Iranian shore of the Persian Gulf has indicators (Saeedi, 2012; Astani et al., 2012; steeply sloping sections and Arabian shore is mostly Mohammad Karami et al., 2014). Despite the high sedimentary (Siebold, 1973). In most of the Persian diversity in the Persian Gulf, little is known about Gulf water salinity is more than 39 psu (Sheppard et subtidal mollusc species of mentioned area both in al., 2010). Depth of the Persian Gulf is 35m in terms of biodiversity and ecology. Some studies on average and maximum depth of 90m and in the Strait molluscs of the Iranian coasts of the Persian Gulf have of Hormuz exceed 100m (Pous et al., 2004). been conducted (e.g. Tadjallipour, 1974; Rezai et al., Biologically, the Persian Gulf is impoverished 1995; Hosseinzadeh et al., 2001; Sadeghi Nassaj et al., because of harsh environmental conditions as well as 2010; Shokat et al., 2010; Asgari et al., 2012), but * Email: [email protected] mostly focused on specimens greater than about 5 mm 37 Amini Yekkta et al. / Distribution of Molluscs in the Eastern Persrsian Gulf, PG-Goos Cruise in size and, therefore, study on small species has Abu Musa, Farur, Siri, Kish, Hendorabi and Lavan always been neglected. Islands. Stations varied from 13 to 90 m in depth The PG-GOOS (the Persian Gulf and Gulf of (Table 1). Oman Oceanographic Study )cruise was launched in October 2012 aboard Nayband Hydrography Vessel to 2.2. Field Sampling cover the oceanographic data gap in the Iranian side of the Persian Gulf and the Gulf of Oman by collecting Sampling was done in Occt-Nov 2012 with a 250 marine physical, chemical, geological, biological and cm2 Van Veen grab in 3 replications in each site. environmental data as well as meteorological Twenty nine stations were sampled in this cruise. parameters. In biological section, macro- and meio- Samples were sieved throughh 1 mm mesh and fixed in benthic inverteebbrates, phytoplankton and zooplankton 10% neutralized formalin. By using stereomicroscope, communities were studied. The present study is focuseed mollusc specimens as well as other benthic groups on the eastern part of the Persian Gulf. were sorted and abundance and diversity of specimens were calculated. By using reliable local references, 2. Materials and Methods samples were identified up to possible taxonomic level. Species which could not be identified, were 2.1. Study Area designated temporary code names to be included in analyses as separate species until further efforts on Twenty nine stations from Bushehr to the Strait of their identification. Factors such as salinity, sediment Hormuz were sampled (Fig. 1). The study arrea temperature, total organic matter (TOM; Heiri et al., included Iranian islands of the Persian Gulf such as 2001) and sediment grain size (Laser particle analyzer, Homuz, Qeshm, Larak, Greater Tonb, Lesser Tonb, Fritsch) were measured as well.

Fig. 1: Sampling stations, Eastern part of the Persian Gulf, 2012

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Table 1. Geographical coordinates for sampling stations pattern in assemblage structure of mollusc. Species Latitude Longitude Depth diversity was evaluated with diversity indices including Stations (N) (E) (m) Shannon–Wiener, Simpson’s and Margalef’s as well as 125 27° 05' 44.8" 56° 22' 14.2" 13 Buzas and Gibson’s evenness measure using PAST 128 26° 50' 17.4" 56° 26' 29.7" 59 software (Hammer et al., 2008). Correlation between 130 26° 41' 33.2" 56° 28' 43.4" 68 environmental factors and mollusc diversity and 123 26° 40' 34.9" 56° 20' 53.5" 71 abundance was assessed to identify the environmental 121 26° 50' 42.9" 56° 15' 42.5" 49 factors that best explained the spatial variation in A 26° 39' 21.5" 56° 04' 56.4" 60 mollusc assemblages (SPSS program version 17). 118 26° 28' 03.0" 55° 55' 24.6" 59 116 26° 37' 11.7" 55° 49' 31.4" 34 3. Results B 26° 29' 28.9" 55° 33' 41.9" 21 TS 26° 12' 26.8" 55° 09' 26.9" 107 In total, 2565 mollusc specimens including 2043 114 26° 04' 41.1" 55° 16' 35.5" 85 gastropods, 515 bivalves and 7 scaphopods were C 25° 54' 47.8" 55° 07' 22.0" 68 108 26° 07' 10.0" 54° 55' 47.0" 85 sampled. Gastropods constituted 80% of molluscs. 106 26° 21' 40.0" 54° 50' 30.5" 63 The abundance of molluscs averaged 1398.36 98 26° 27' 47.2" 54° 28' 29.7" 27 (±261.95) ind./m2. Among stations, station C 99 26° 19' 44.4" 54° 28' 10.0" 79 (located near Abu Musa Island) with an average 101 26° 03' 27.8" 54° 27' 32.1" 81 abundance of 8040 (±1625.30) ind./m2 was the most 102 25° 54' 10.2" 54° 27' 25.9" 74 abundant site followed by station 114 (5600 104 25° 40' 48.6" 54° 25' 23.5" 59 ±1785.72 ind./m2). No mollusc specimens were D 25° 43' 53.9" 54° 05' 23.5" 63 found in station situated near Lesser Tonb (TS), the E 26° 34' 49.2" 54° 00' 27.3" 26 deepest station (107 m; Fig. 2). 88 26° 35' 02.1" 53° 49' 42.3" 54 Excluding stations G and 90, gastropods dominated 90 26° 19' 08.0" 53° 47' 54.6" 90 molluscs in all stations. Scaphopods were just found in 92 26° 03' 13.0" 53° 45' 51.2" 75 F 26° 40' 11.8" 53° 40' 34.3" 20 stations 102 and 130. The most abundant gastropod 84 26° 41' 16.5" 53° 36' 25.2" 58 taxa were species of genus Costellaria and the most G 26° 44' 34.8" 53° 12' 58.3" 84 abundant bivalve species was Ervilia scaliola. Atys 71 27° 22' 25.9" 52° 30' 32.5" 63 cylindrica in gastropods and Nuculoma layardii in 67 27° 35' 54.6" 52° 07' 08.7" 72 bivalves had the widest distribution in sampling the area; they were present in 21 and 7 out of 29 stations, 2.3. Data Analysis respectively. Kruskal-Wallis test yielded significant differences in Plots of average molluscs abundance were analyzed abundance of molluscs in different stations (p<0.05). using EXCEL 2007. Kruskal-Wallis test (SPSS Cluster analysis based on similarities in their program version 17) was used for the differences in assemblage structure, separated station TS from other mollusc abundance among sites as normality could not stations since no mollusc specimens were reported from be obtained by transformation. Cluster analysis based this station. In about 43% similarities, two other groups on Bray- Curtis similarity matrix of fourth root- are formed clearly that nearly separate stations located transformed abundance data was used in PRIMER 5 around Larak, Hormuz and Qeshm Islands from other (Clarke and Warwick, 1994) to depict the spatial stations (Fig. 3).

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Fig. 2: Average density (ind./m2) of molluscs in different stations

Fig. 3: Cluster analysis based on Bray- Curtis similarity matrix of fourth root- transformed abundance data

40 Journal of the Persian Gulf (Marine Science)/Vol .5/No .17/September 2014/ 11 / 37-48

In total, 84 mollusc taxa were identified (±0.28) psu. The sediment temperature ranging (Appendices I and II), including 60 gastropod (36 between 21.50 °C (stations 90 and G) and 28 °C taxa up to species, 18 taxa up to genus, and 5 taxa up (station B), averaged 25.02 (±0.37)°C. TOM content to family levels), 23 bivalve (13 taxa up to species, 6 of sediments was in range of 4.50% in station F to taxa up to genus, and 4 taxa up to family levels) and 16.75% in station A. Sampling area covered 13 to 90 1 scaphopod (up to family level). m depth (60.93±4.30 m). Excluding stations 114 (90% However, few species remained unidentified. pebble), in other station silt constituted the highest Station C with 40 taxa was the most diverse station, percentage of the grain size categories (Table 3). followed by station 114 with 39 taxa. The highest The average abundance of molluscs were values for Shannon index of diversity (2.90) and significantly correlated with depth, sediment Margalef’s index of richness (6.35) were seen in temperature (p<0.01), salinity and TOM (p<0.05). station 114 with sediments mostly (90%) in range of Meanwhile, sediment temperature and TOM were pebble size. Station F showed the highest Simpson negatively correlated with the average abundance of value (0.92). Average values for Shanon and molluscs. In addition, significant correlation was Simpson indices were 2.08 (±0.11) and 0.81 (±0.02), observed between Shanon values and sediment respectively. In most stations mollusc individuals temperature, salinity, depth (p<0.05) and TOM were evenly distributed among different taxa (p<0.01). Mollusc diversity also showed negative (0.71±0.04; Table 2). correlation with the sediment temperature and TOM, Salinity varied between 36.46 psu (station B) and Environmental factors showed significant correlation 41.40 psu (station 99) with an average of 39.20 with abundance and diversity of mollusks (Table 4). Table 2. Diversity indices in different stations Station Taxa Dominance Simpson Shannon Evenness Individuals Margalef (S) (D) (1-D) (H) (e^H/S) 125 7 11 0.21 0.79 1.77 0.84 2.50 128 7 8 0.16 0.84 1.91 0.96 2.88 130 9 12 0.14 0.86 2.09 0.90 3.22 123 7 10 0.18 0.82 1.83 0.89 2.61 121 14 35 0.13 0.86 2.30 0.72 3.66 A 1 1 1.00 -* -* 1.00 -* 118 14 68 0.31 0.69 1.62 0.36 3.08 116 10 26 0.21 0.79 1.85 0.64 2.76 B 3 3 0.33 0.67 1.10 1.00 1.82 114 39 398 0.08 0.91 2.90 0.47 6.35 C 40 603 0.12 0.88 2.64 0.35 6.09 108 21 68 0.09 0.91 2.71 0.71 4.74 106 3 10 0.36 0.64 1.05 0.96 0.87 98 1 1 1.00 -* -* 1.00 -* 99 8 21 0.26 0.74 1.65 0.65 2.30 101 19 45 0.10 0.89 2.59 0.70 4.73 102 16 42 0.11 0.89 2.46 0.73 4.01 104 16 33 0.12 0.88 2.43 0.71 4.29 D 12 37 0.14 0.86 2.20 0.75 3.05 E 2 2 0.50 0.50 0.69 1.00 1.44 88 10 36 0.16 0.84 2.01 0.74 2.51 90 28 346 0.31 0.69 1.97 0.26 4.62 92 14 64 0.14 0.86 2.25 0.67 3.13 F 30 100 0.08 0.92 2.86 0.58 6.30 84 8 16 0.15 0.85 1.98 0.91 2.52 G 36 344 0.17 0.83 2.53 0.35 5.99 71 17 74 0.13 0.87 2.32 0.60 3.72 67 22 125 0.14 0.86 2.40 0.50 4.35 * due to low abundance, indices could not be analyzed

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Table 3. Environmental factors in sampling stations Sediment Stations temperature Salinity (psu) Sand (%) Clay (%) Silt (%) TOM (%) (°C) 125 27.5 37.07 13.2 84.6 2.2 10 128 23 36.56 14.4 85.3 0.3 11.25 130 24.5 38.18 16.5 83.5 0 11.75 123 24.5 38.37 34.5 65.4 0.1 7 121 24 37.28 10 90 0 9.50 A 26 38.10 23.3 76.7 0 16.75 118 26 38.25 31 69 0 11.75 116 27 36.58 20 80 0 9.750 B 28 36.46 0 98.5 1.5 10.50 TS missing 39.88 25.6 74.3 0.1 missing 114 24.5 39.70 4 6 0 5.50 C 24 39.55 18.2 80.6 1.2 5.25 108 24 40.22 15 84.4 0.6 9.75 106 26 38.35 32.5 65 2.5 14.75 98 27.5 38.90 20 78.5 1.5 14.25 99 26 41.40 23 77 0 14.25 101 27.5 40.80 19 80 1 6.50 102 26.5 40.80 34 66 0 10 104 25 39.70 33.5 66.5 0 8.50 D 24 39.98 22 78 0 9.75 E 27 39.75 28 72 0 9 88 26.5 missing 39.8 60.1 0.1 13 90 21.5 40.73 20 80 0 10 92 22 40.68 35 64.5 0.5 14 F 26 38.51 21 78 1 4.50 84 22.5 40.54 18.1 81.8 0.1 13.50 G 21.5 40.60 4.7 95.1 0.2 8 71 23 40.04 23 76.4 0.6 14.50 67 23 40.37 missing missing missing 16.50 25.02 74.90 0.48 Average 39.20 (±0.28) 21.40 (±1.88) 10.70 (±0.63) (±0.37) (±3.09) (±0.13)

Table 4: Spearman’s correlation between abundance and diversity of molluscs and environmental factors Environmental Factors Sediment Temp. Salinity (psu) Depth TOM

** * ** * Average Correlation Coefficient -0.498 0.474 0.536 -0.489

abundance Sig. 0.010 0.014 0.005 0.011

Correlation Coefficient -0.413* 0.397* 0.450* -0.63** Shannon index Sig. 0.036 0.045 0.021 0.0

* Correlation is significant at the 0.01 level ** Correlation is significant at the 0.05 level

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4. Discussion affecting mollusc abundance. Spatial and temporal distribution and abundance Samples represented 60 gastropod taxa (36 taxa of organisms are central to ecology (Kaarn, 2010). up to species, 18 taxa up to genus, and 5 taxa up to Therefore, understanding the mechanisms that govern family levels), 23 bivalves (13taxa up to species, 6 species’ distributions is the first step to improve the taxa up to genus, and 4 taxa up to family levels) and ecological theory and species management. Predicting 1 scaphopod (up to family level) (Appendices I and the impacts of future climate change on Earth’s II). Sixty gastropod species along with 57 bivalve biodiversity is critical to preserve biological resources species have been recorded from Kuwait Bay and and for understanding evolutionary processes (Saupe surrounding waters (Al-Yamani et al., 2009). Al- et al., 2014), which is not possible without basic Yamani et al. (2012) reported 130 gastropod and 99 information about species distribution and diversity. bivalve species from Kuwait. They included littoral Therefore, there is a need to enrich database on species and their sampling was performed in an 8- distribution of macrobenthic species of the Persian year period, which can explain the higher diversity Gulf in space and time and to identify the influential compared with the present study. factors that explain the variation in their assemblages Several factors might be correlated with the to be able to manage this unique ecosystem in a distribution of benthic invertebrates; for instance, proper way. sedimentation (Harrison et al., 2007), grain size (Mayoral, 2011; Lourido et al., 2010; Garmendia et Acknowledgements al., 2008; Coleman et al., 1997; Sanders, 1958), substrate stability (Mayoral, 2011), depth (Coleman This study was supported by the Iranian National et al., 1997), temperature, pH, CO2 pressure and Institute for Oceanography and Atmospheric Science calcium saturate (Byrne, 2011). (INIOAS). Authors are indebted to all scientists as Among environmental factors that have been well as support and nautical staff in PG-GOOS correlated with benthic abundance, Hale (2012) cruise who made this study possible. found temperature the most effective one in benthos distribution. In present study, sediment temperature References and TOM are negatively correlated with diversity and average abundance of mollsucs (Table 4), which Al-Yamani, F., Boltachova, N., Revkov, N., Makarov, is in accordance with other studies (Mohammadi M., Grintsov, V., Kolesnikova, E., and Murina, G. Roozbahani et al., 2010; Shirmohammadi et al., V., 2009. Winter species composition, diversity and 2012). Kumar and Khan (2013) reported salinity and abundance of macrozoobenthos in Kuwait’s waters, pH with significant correlation with benthos Persian Gulf. ZooKeys, 31: 17-38. diversity (p<0.05). They also stated that there existed Al-Yamani, F. Y., Skryabin, V., Boltachova, N., significant negative correlation between TOM and Revkov, N., and Makarov, M., 2012. Illustrated Dominance index for benthic fauna (p<0.01). Atlas on the Zoobenthos of Kuwait. Kuwait In all 8 stations, which have been separated from institute for scientific research, 401 p. others as a result of cluster analysis (Fig. 3), silt Asgari, M., Amini Yekta, F. and Izadi, S., 2012. dominated the sediments (about 80%; Table 3). Dominant intertidal crustacean and gastropod Significant correlation was also found among species in Qeshm Island, Iran, northern Persian stations with regard to their grain size (p<0.01). It is Gulf. Marine Biodiversity Records, 5: 1-8. suggested that sediment texture is an important factor Astani, M., Vosoughi, A.R., Salimi, L. and Ebrahimi,

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M., 2012. Comparative study of heavy metal (Cd, Heiri, O., Lotter, A. F. and Lemcke, G., 2001. Loss Fe, Mn, and Ni) concentrations in soft tissue of on ignition as a method for estimating organic and gastropod Thais mutabilis and sediments from carbonate content in sediments: reproducibility intertidal zone of Bandar Abbas. Advances in and comparability of results. Journal of Environmental Biology, 6(1): 319-326. Paleolimnology, 25: 101-110. Barnes, R.S.K., Calow, P.P., Olive, P.J.W., Golding, Hosseinzadeh, H., Daghoghi, B. and Rameshi, H., D.W. and Spicer, J.I., 2009. The invertebrates: a 2001. Atlas of the Persian Gulf molluscs. Tehran: synthesis. John Wiley & Sons. 472P. Iranian Fisheries Research Organization, 208 P. Byrne M., 2011. Impact of ocean warming and ocean Kraan, C., 2010. Spatial ecology of intertidal acidification on marine invertebrate life history macrobenthic fauna in a changing Wadden Sea. stages: vulnerabilities and potential for persistence PhD Thesis, University of Groningen, Groningen, in a changing ocean. Oceanography and Marine the Netherlands. Biology: An Annual Review, 49: 1–42. Kumar, P.S., Khan, A.B., 2013. The distribution and Clarke, K.R. Warwick, R.M., 1994. Changes in diversity of benthic macroinvertebrate fauna in marine communities: an approach to statistical Pondicherry mangroves, India. Aquatic Biosystems, analysis and interpretation. Plymouth Marine 9(1): 15. Laboratory, UK, 144 p. Lourido A., Moreira J. and Troncoso J.S., 2010. Spatial Coleman N., Gason A.S.H. and Poore G.C.B., 1997. distribution of benthic macrofauna in subtidal High species richness in the shallow marine waters sediments of the Ría de Aldán (Galicia, northwest of south-east Australia. Marine Ecology Progress Spain). Scientica Marina, 74 (4): 705–715. Series, 154: 17-26. Mayoral H., 2011. Particle size, critical shear stress, Garmendia M., Borja A. and Muxika I., 2008. Long- and benthic invertebrate distribution and term environmental, climatic and anthropogenic abundance in a gravel-bed river of the southern factors affecting subtidal soft-bottom benthic Appalachians. Geosciences Thesis, Georgia State communities, within the Basque coast. Revista de University. Paper 31. Investigación Marina, 2: 28 pp. Mohammad Karami, A., Riyahi Bakhtiari, A., Hale S.S., 2012. Spatial patterns of subtidal benthic Kazemi, A. and Kheirabadi, K., 2014. Assessment invertebrates and environmental factors in the of Toxic Metals Concentration using Pearl Oyster, nearshore Gulf of Maine. Chapter 13, Advancing Pinctada radiata, as Bioindicator on the Coast of an Ecosystem Approach in the Gulf of Maine. Persian Gulf, Iran. Iranian Journal of Toxicology, American Fisheries Society Symposium. 7(23): 956-961. American Fisheries Society, Bethesda, MD, Mohammadi Roozbahani, M., Nabavi, S.M., 79:167-183. Farshchi, P. and Rasekh, A., 2010. Studies on the Hammer, Ø., Harper, D.A.T. and Ryan, P.D., 2008. benthic macroinvertebrates diversity species as PAST- Palaeontological Statistics, ver. 1.87. bioindicators of environmental health in Bahrekan Harrison E.T., Norris R.H. and Wilkinson S.N., Bay (Northwest of Persian Gulf). African Journal 2007. The impact of fine sediment accumulation of Biotechnology, 9(39). on benthic macroinvertebrates: implications for Pous, S.P., Carton, X. and Lazure, P., 2004. river management. In: Proceedings of the 5th Hydrology and circulation in the Strait of Hormuz Australian Stream Management Conference. and the Gulf of Oman-Results from the GOGP99 Australian rivers: making a difference. Charles Experiment: 1. Strait of Hormuz. Journal of Sturt University, Thurgoona, New South Wales. Geophysical research, 109(C12), C12037.

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Appendix I: List of mollusc taxa identified in present study up to genus or species level.

Gastropoda Hypermastus sp. Eulimella venusta Septifer ?bilocularis

Pseudominolia sp. Zafra comistea Miralda scopulorum Lucina dentifera

Priotrochus sp. Zafra selasphora Odostomia eutropia Amphilepida sp.

Lodderia novemcarinata Zafra sp. Pyrgulina callista Carditopsis majeeda

Morchiella moreleti Mitrella agatha Syrnola sp. Tellina nites

Cyclostrema archeri Nassarius himeroessa Turbonilla linjaica Tellinides emarginatus

Cyclostrema sp. Nassarius spp. Pupa affinis Tellina sp.

Truncatella ?marginata Bullia persica Bullina lineata Cadella semen

Pseudonoba sp. Ancilla farsiana Atys cylindrica Ervilia scaliola

Stosicia annulata Ancilla sp. Atys pellyi Timoclea arakana

Gibberula cf. Voorwindia tiberiana Retusa spp. Pitar sp. mazagonica

Rissoina sp. Granulina oodes Ringicula propinquans Corbula sulculosa

Argyropeza divina Ziba pretiosa Tornatina inconspicua Corbula erythraeensis

Cerithidium sp. Costellaria spp. Cylichna collyra Thracia adenensis

Turritella sp. Splendrillia spp. Bivalvia Scaphopoda

Atlanta peronii Daphnella ?thia Solemya africana Dentalium sp.

Natica vitellus Terebra sp. Nuculoma layardii

Natica sp. Mothilda telamonia Nuculana sp.

Epitonium spp. Mothilda gracillima Arca sp.

Niso venosa Chrysallida cf fischeri Modiolus sp.

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Appendix II: Some mollusc taxa identified in this project..

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