Sea sonal vari a tions, en vi ron men tal pa ram e ters and stand ing crop as sess ment of ben thic foraminifera in east ern Bah rain, Ara bian Gulf
Mu ham mad ARSLAN1, *, Mi chael A. KAMINSKI1, Bassam S. TAWABINI1, Mu ham mad ILYAS2, Lamidi O. BABALOLA2 and Fabrizio FRONTALINI3
1 King Fahd Uni ver sity of Pe tro leum and Min er als, Geosciences De part ment, Col lege of Pe tro leum En gi neer ing and Geosciences, PO Box 701, Dhahran, 31261, Saudi Ara bia
2 King Fahd Uni ver sity of Pe tro leum and Min er als, Re search In sti tute, Dhahran, 31261, Saudi Ara bia
3 Universit´ degli Studi di Urbino “Carlo Bo”, Cam pus Scientifico, Localit´ Crocicchia 61029, Urbino, It aly
Arslan, M., Kaminski, M.A., Tawabini, B.S., Ilyas, M., Babalola, L.O., Frontalini, F., 2016. Sea sonal vari a tions, en vi ron men tal pa ram e ters and stand ing crop as sess ment of ben thic foraminifera in east ern Bah rain, Ara bian Gulf. Geo log i cal Quar terly, 60 (1): 26–37, doi: 10.7306/gq.1242
Liv ing ben thic foraminifera in a rel a tively un pol luted site off shore Bah rain in the Ara bian Gulf, were stud ied to de ter mine the sea sonal vari abil ity of their pop u la tions, as well as en vi ron men tal pa ram e ters that may af fect their dis tri bu tion. The max i mum foraminiferal den sity was ob served dur ing win ter with the as sem blages pri mar ily dom i nated by rotaliids and sec ond arily by miliolids. The high pop u la tion is at trib uted to an in creased num ber of ju ve niles. A re la tion ship be tween sed i ment grain-size and the foraminiferal den sity re veals that ju ve niles were most abun dant on coarse-grained sandy sub strate and less abun - dant on fine-grained sub strates. In spring, the foraminiferal den sity de creased, and the low est val ues were ob served dur ing sum mer. The pop u la tion in creased again in au tumn with high est ju ve nile/adult ra tios. More over, re sults of rel a tive abun - dance and spe cies con sis tency show that Am mo nia and Glabratellina are con sis tent from the shal low est to the deep est sta - tion, whereas miliolids oc curred only at deeper sta tions. The num bers of Peneroplidae and Elphidium also in creased along the depth transect. En vi ron men tal char ac ter iza tion re veals that al though the site is sub ject to eutrophication caused by ni - trates and sul fates, pol lu tion caused by hy dro car bons and heavy met als is not sig nif i cant. The as sess ment of 63 heavy met - als showed that none of the met als had con cen tra tions that ex ceed in ter na tion ally ac cepted norms (the de vised level of Ef fect Range – Low), but with high con cen tra tion of stron tium. The lack of a sig nif i cant en vi ron men tal ef fect of heavy met als is con firmed by the Foraminiferal Ab nor mal ity In dex of <2%. Like wise, no hy dro car bon con tam i na tion was de tected in the wa ter or sed i ment sam ples. We con clude that the site in Bah rain is not yet ad versely af fected by hu man de vel op ment, and there fore can pro vide base line in for ma tion for fu ture com par i son and as sess ment of foraminiferal as sem blages in con tam i - nated zones of the Ara bian Gulf.
Key words: Ara bian/Per sian Gulf, ben thic foraminifera, stand ing crop, east ern Bah rain.
INTRODUCTION
Ben thic foraminifera rep re sent a di verse group of ma rine protists that are ubiq ui tously dis trib uted in ma rine and tran si - tional ma rine hab i tats (Murray, 1991). Their dis tri bu tional pat - terns are gen er ally de pend ent on both en vi ron men tal con di - tions and sea sonal vari a tions (Murray, 2006; Sarita et al., 2015). Their as sem blages re flect en vi ron men tal gra di ents such as wa ter depth, physicochemical pa ram e ters of wa ter, sub - strate pa ram e ters, avail abil ity of nu tri ents, and the ef fects of anthropogenic pol lu tion, in ad di tion to nat u ral sea son al ity re - lated to their re pro duc tive cy cle (Murray, 2006; Sarita et al.,
2015). Ben thic foraminifera have been widely used to study en - vi ron men tal changes in mar ginal ma rine, coastal and ma rine shelf en vi ron ments (i.e. see re view in Murray and Alve, 2002).
For ex am ple, Sarita et al. (2015) il lus trated en vi ron ment spe - cific spa tial and sea sonal dis tri bu tion of liv ing ben thic foraminifera in the es tu ary of Guadiana (south east ern Por tu - gal). In an other ex am ple, Frontalini et al. (2009) re ported low di - ver sity ben thic foraminiferal as sem blages in the la goon of Santa Gilla (It aly) af fected by in dus trial, ag ri cul tural, and do - mes tic dis charges. Ben thic foraminifera have been widely used as bioindicators and for as sess ing the health of ma rine eco sys - tem as con se quences of pol lu tion (Alve, 1995; Yanko et al., 1998; Armynot du Châtelet and Debenay, 2010; Frontalini and Coccioni, 2011).
The west ern part of the Ara bian Gulf is the world’s larg est hypersaline sea (John et al., 1990), and as such it of fers unique ma rine hab i tats to foraminiferal as sem blages. The his tory of foraminiferal study in the Ara bian Gulf is not new and their dis tri - bu tional pat terns, tax on omy, and ecol ogy have been largely in - ves ti gated (Murray, 1965a, b; 1966a, b, c, d; 1991; Haake,
* Corresponding author, e-mail: arsilan324@gmail.com Received: March 5, 2015; accepted: July 7, 2015; first published online: July 14, 2015
1970; Lutze, 1974; Basson and Murray, 1995; Cherif et al., 1997). How ever, hu man ac tiv i ties are now pos ing ma jor treat on the Ara bian Gulf coastal en vi ron ments, both on shore and off - shore. Coastal veg e ta tion (man groves) in the area has been al - ready af fected by hu man ac tiv i ties (Hamza and Munawar, 2009). Ex ten sive hu man ac tiv i ties also dis turbed large ar eas along the Saudi Ara bian and U.A.E. coast lines, and now many of Murray’s (1966a, b, c, d) orig i nal sam ple lo cal i ties along the U.A.E. coast are lo cated be neath park ing lots (F. Fiorini, pers.
comm., 2011). Fur ther more, as the Ara bian Gulf is ex ploited as one of the main oil pro duc ing re gions of the world, more than half of the world’s pe tro leum is trans ported through the Gulf (Oostdam, 1980). As a re sult, hy dro car bon drill ing ac tiv i ties com bined with ex ten sive ur ban iza tion are sys tem at i cally dis - turb ing coastal ar eas (Coles and McCain, 1990; Burt, 2014).
The un der stand ing of the foraminiferal dis tri bu tional pat - terns re quires con sid er ation of a broad range of sea sonal and en vi ron men tal fac tors. Stud ies elu ci dat ing the ef fects of tem po - ral vari a tions on ben thic foraminiferal as sem blages are few and are mostly based on stand ing crop as sess ment with out as sess - ing the ef fects en vi ron men tal pa ram e ters (Basson and Murray, 1995; Scott et al., 1995). Basson and Murray (1995) re ported tem po ral vari a tions of four intertidal foraminiferal spe cies in a la - goon from west ern Bah rain, whereas Scott et al. (1995) pre - sented tem po ral vari a tions of ben thic foraminiferal as sem - blages un der aquaculture op er a tions. How ever, there is a still need to doc u ment and in fer the role of en vi ron men tal fac tors cou pled with sea sonal vari a tions from an un dis turbed area.
Fur ther more, it is es sen tial to es tab lish base line stud ies of foraminiferal as sem blages for fu ture en vi ron men tal as sess - ment, and to pro vide con trols for mon i tor ing the ef fects of anthropogenic ac tiv i ties that threaten ma rine eco sys tems.
The pres ent study aims to (a) doc u ment the sea sonal vari a - tions of foraminiferal den sity (FD) and dis tri bu tion of liv ing ben - thic foraminifera in a coastal area of east ern Bah rain; and (b) en vi ron men tally char ac ter ize the study area by eval u at ing the pol lu tion lev els and the eco log i cal qual ity of the area.
STUDY AREA
The study was con ducted south of the town of Askar, a fish - ing vil lage on the east ern coast of Bah rain (Fig. 1A, B). The lo - cal ity was se lected be cause it is lo cated in a pro tected cove next to the Bah rain De part ment of Fish er ies re search sta tion, and there fore rel a tively un dis turbed by hu man ac tiv i ties. The sam ple lo cal ity is just off shore from a small la goon that was orig i nally in ves ti gated for foraminifera by Basson and Murray (1995). This la goon, which par tially lies within the prop erty of the re search sta tion rep re sents the only site within the King dom of Bah rain that has been pre vi ously stud ied for foraminifera, and has be come known to our re search group as “Murray’s Pool”
(Amao, 2014). The fore shore to off shore transect off “Murray’s Pool”, lo cated at 26°02’37.11" N, 50°37’32.77" E, was sam pled for this study (Fig. 1C).
The coastal area of east ern Bah rain is microtidal (<1 m) with a di ur nal rhythm (Basson et al., 1989). The fore shore is wide, slopes very gently, and is char ac ter ized by a soft, silty, sandy car bon ate sed i ment ve neer dis con tin u ously over ly ing lithified hard-ground (Basson and Murray, 1995). Fur ther more, the fore shore is oc ca sion ally cov ered with a bloom of an al gal mat
spread ing over the sed i ments, par tic u larly dur ing sum mer, with iso lated patches of sea grass be gin ning about 50 m from the shore line. On the east ern side of Bah rain, wa ter tem per a ture var ies be tween 17.5°C in win ter to 36.6°C in sum mer, whereas sa lin ity re mains mostly con stant through out the year, i.e. 45–46 (Basson et al., 1989; Basson and Murray, 1995).
MATERIALS AND METHODS
SAMPLING STRATEGY
In or der to as sess the sea sonal ef fects, five sam ples were col lected dur ing four sea sons (i.e., win ter, spring, sum mer and au tumn), from the fore shore area along the depth transect off - shore from “Murray’s Pool” (Fig. 1C). Sam pling sites were placed at 17, 50, 125, 200 and 250 m from the shore and lo ca - tions were de ter mined by GPS. The win ter sam pling was car - ried out in late De cem ber 2013, fol lowed by a spring sur vey in early March 2014, a sum mer one at the end of May 2014, and an au tumn one in early Oc to ber 2014. The whole study com - prised 20 intertidal bot tom wa ter and sed i ments from wa ter depths of 35 cm to 1.2 m (Ap pen dix 1*).
Bot tom wa ters were sam pled by dip ping well-rinsed glass jars at each sta tion prior to the sed i ment sam pling to avoid any al ter ation of physicochemical pa ram e ters. Sed i ment sam ples with a depth of ~1.2 cm (vol ume ~57.6 cm3) were col lected with a spat ula tak ing care not to dis turb the sed i ment floor, and placed into plas tic stor age boxes fit ted with a lid that was se - cured un der wa ter. A layer of alu mi num foil was placed over the jar mouth to avoid sed i ment con tact with the plas tic cap. Both wa ter jars and sed i ments boxes were im me di ately trans ported to the lab o ra tory for anal y sis. Sam ple pro cess ing was car ried out at the Re search In sti tute and En vi ron men tal Sci ences labs at King Fahd Uni ver sity of Pe tro leum and Min er als (Saudi Ara - bia). Sed i ment and wa ter sam ples used for the char ac ter iza tion of the en vi ron men tal qual ity (eutrophication in di ca tors, heavy met als and hy dro car bons) were only analysed dur ing the win ter sea son.
BENTHIC FORAMINIFERA ANALYSIS
In the lab o ra tory, 5 cm3 of sed i ment was taken from each box. Each sam ple was care fully washed with sea wa ter through a 63 µm mesh sieve. Fi nally, the en tire res i due was mi cro scop i - cally ana lysed and the to tal num bers of liv ing foraminifera (both adults and ju ve niles) were wet-picked un der a re flected-light bin oc u lar mi cro scope based on the pres ence of pro to plasm.
We vi su ally dis tin guished “liv ing” (pro to plasm-filled tests ex cept in the last cham ber) from “dead” (pro to plasm-empty or de - graded) as de scribed pre vi ously (Ortiz et al., 1995).
Foraminiferal as sem blage pa ram e ters of the stand ing crop were cal cu lated, in clud ing the adult/ju ve nile (A/J) ra tio (in di vid - u als with di am e ter less than 150 µm were con sid ered as ju ve - niles), foraminiferal den sity (FD – num ber of liv ing in di vid u als per 5 cm3), ge neric di ver sity (“rich ness”, S), foraminiferal dom i - nance (D), and fau nal con stancy (Fc n
= N ´ 100, where: n – the num ber of sam ples where the spe cies oc curs, N – the to tal of sam ples col lected). Foraminifera were tax o nom i cally iden ti fied
* Supplementary data associated with this article can be found, in the online version, at doi: 10.7306/gq.1242
at ge nus level for ju ve niles and at spe cies level for adults with the aim to un der stand the to tal stand ing crop and spe cies rep - re sen ta tion dur ing each sea son. Tax o nom i cal iden ti fi ca tion was car ried largely fol low ing the mono graphs of Hottinger et al.
(1993), Loeblich and Tappan (1994) and Hay ward et al. (2004).
Be cause much of the as sem blages con sisted of ju ve niles, we did not at tempt to re solve the spe cies tax on omy. Group di ver - sity was fur ther as sessed by the Fischer a in dex and the Shan - non di ver sity in dex (H'= -
å
pi ´lnpi; Shan non, 1948; Shan - non and Weaver, 1963) as well as even ness (J), and equitability (E). The above men tioned di ver sity in di ces werecal cu lated us ing the PAST – PAlaeontological STa tis tics data anal y sis pack age (ver sion 1.68). The di ver sity in di ces were de - rived to com pare be tween sam ples in this study and are not com pa ra ble to stud ies that have re ported spe cies level di ver sity in di ces. There fore, the di ver sity in dexes must be con sid ered with care be ing cal cu lated at the group level. Lastly, Foraminiferal Ab nor mal ity In dex (FAI) was cal cu lated to pos si - bly doc u ment the ef fect of pol lu tion (Frontalini and Coccioni, 2008). The most im por tant foraminiferal spe cies were pho to - graphed us ing a scan ning elec tron mi cro scope (SEM).
Fig. 1. Geographical context of “Murray’s Pool” in the Arabian Gulf
A – the Arabian Gulf; B – location map showing study area in eastern Bahrain; C – the depth transect with sampling locations
PHYSICOCHEMICAL PARAMETERS OF WATER
Sa lin ity, tem per a ture, and pH were mea sured in situ us ing YSI multi-probe dur ing each sam pling pe riod. How ever, con - duc tiv ity, bi car bon ate al ka lin ity, and tur bid ity were eval u ated in the lab o ra tory us ing PC-BODTM Stand Alone Sys tem (MANTECH-YSI probes) by run ning sam ples in du pli cates.
GRAIN-SIZE ANALYSIS
In or der to de ter mine the grain-size dis tri bu tion of the sed i - ments along the transect, sam ples were treated ini tially with an H2O2 so lu tion to re move the or ganic mat ter. Af ter wards, stan - dard anal y sis was per formed by tak ing 50 grams of each sam - ple fol lowed by man ual siev ing and dry ing at 60°C. The grain-size dis tri bu tions were sta tis ti cally and graph i cally sum - ma rized to un der stand the po ros ity and per me abil ity for later anal y sis (ASTM, 1984).
TOTAL ORGANIC CARBON (TOC) ANALYSIS
For TOC anal y sis, ap prox i mately 200 mg of the dried and ground sam ple was weighed and placed in ce ramic boats. Af ter - wards, sam ple was sus pended in a di luted hy dro chlo ric acid so - lu tion thrice a day to break down all the car bon ates pres ent in the sam ple re sult ing into re moval of to tal in or ganic car bon (TIC).
Lastly, the sus pen sions were in jected and ana lysed in Shimadzu TOC-Vcsh To tal Or ganic Car bon An a lyzer for TOC anal y sis.
Stan dards and sam ples were weighed in du pli cates and five cal i - bra tion points were taken for draw ing a cal i bra tion curve.
EUTROPHICATION POLLUTION ANALYSIS
The eutrophication in di ca tors (SO4 2 - , PO4
2
- , NO–3 and NO–2) were de tected by us ing Ion chro ma tog ra phy (IC - Metrohm 850 Pro fes sional sys tem, Swit zer land). The sea wa ter sam ples were pre pared by per form ing 1000-fold di lu tion in ul tra-pure wa ter.
Prior to anal y sis, the stan dard so lu tions of 10 ppm con cen tra - tion were pre pared for each ion and then in jected into the sys - tem to as sess the per for mance and cal i bra tion of the in stru ment (Paul et al., 2005; Wil son et al., 2011).
HEAVY METALS ANALYSIS
In or der to de ter mine the heavy metal con tents in the sed i - ments, 5 g of each sam ple was dried un der the light bulb at low tem per a ture to pre vent the evap o ra tion of heavy-met als, then re duced to fine pow der. There af ter, the heavy metal con tent was in ves ti gated in all the sed i ments by Ac ti va tion Lab o ra to ries Ltd. (On tario, Can ada, http://www.actlabs.com) that an a lysed a frac tion of 0.5 g of a sam ple for 63 el e ments us ing in duc tively cou pled plasma mass spec trom e try (ICP-MS), which is a multi-el e ment tech nique ca pa ble of mea sur ing con cen tra tions at very low de tec tion lim its (mg/kg to µg/kg). The sam ple ma te - rial was di gested in aqua regia (0.5 ml H2O, 0.6 ml con cen trated HNO3 and 1.8 ml con cen trated HCl) at 90°C in a mi cro pro ces - sor con trolled di ges tion block for 2 hours. The anal y ses were per formed un der stan dard qual ity con trol pro to cols.
HYDROCARBON ANALYSIS
Hy dro car bon ex trac tion from the sed i ments was per formed us ing the ASE 200 ac cel er ated sol vent ex trac tion sys tem, a pro ce dure to ex tract or ganic sol vents at high tem per a ture and pres sure above the boil ing point as de scribed as Method 3545
in U.S. EPA SW-846 Meth ods. In or der to per form this anal y sis, rep re sen ta tive sam ples of 5 g of sed i ments from each sta tion was taken and ho mog e nized equally with com mer cially avail - able hy drant for re moval of mois ture con tent. The mix ture was di rectly en closed into the sam ple cells which were sub se quently in stalled on the sys tem to stat i cally ex tract the hy dro car bons un der 100°C tem per a ture and 500 psi pres sure for 20 min. Fi - nally, com pressed gas al lowed ex trac tion of hy dro car bon from the sam ple cell to the col lec tion ves sel us ing n-hex ane. For qual ity con trol, sam ples were run in du pli cates and sur ro gate spik ing was per formed to as sess the ex trac tion ef fi ciency.
Anal y ses of the ex tracts were per formed us ing gas chro ma - tog ra phy flame ion iza tion de tec tor (GC/FID) Agilent tech nol ogy 7890A GC sys tem. Sep a ra tions were per formed us ing a 30 m ´ 0.32 mm in ter nal di am e ter Varian cap il lary col umn. The car rier gas sup ply was he lium with col umn flow rate of 25 mL/min and the pres sure was reg u lated by hy dro gen and air flow ing at rate of 30 mL/min and 300 mL/min, re spec tively. The col umn tem - per a ture dur ing trans fer was 60°C. It was main tained for 1 min, and then pro grammed at 10°C/min to 150°C for 12 min. The tem per a ture of the flame ion iza tion de tec tor (FID) was 200°C.
Peaks were in te grated us ing a Chrom Card sys tem (CE In stru - ments). Fi nally, quan ti fi ca tion of the to tal hy dro car bon con tent (THC) was cal cu lated us ing a hy dro car bon win dow of C10 to C36 cal i bra tion stan dards.
STATISTICAL ANALYSIS
In or der to de ter mine the as sem blages’ re la tion ship with en - vi ron men tal pa ram e ters, multivariate tech niques prin ci pal com - po nent anal y sis (PCA) and clus ter anal y sis (CA) were per - formed us ing Statistica v6.0. Prior to sta tis ti cal anal y sis, the data were nor mal ized and an ad di tive log a rith mic trans for ma - tion log(1 + X) was per formed to elim i nate the ef fects of or ders of mag ni tude dif fer ences be tween dif fer ent en vi ron men tal vari - ables. The CA was ap plied to iden tify the sim i lar i ties be tween sam pled sta tions. The anal y sis was based on the Eu clid ean dis tance and the Ward’s link age method that pro duced dendrograms with ex cep tion ally well-de fined clus ters (Parker and Ar nold, 2000) where each clus ter in cludes sta tions with a sim i lar spa tial dis tri bu tion pat tern (Samir et al., 2003). The PCA at tempts to rec og nize the re spon si ble fac tors ex plain ing pat tern of cor re la tion within a set of ob served vari ables. In a PCA, it is also pos si ble to com pute ad di tional vari ables (bi otic data) which do not con trib ute to the re sults.
RESULTS
ENVIRONMENTAL CHARACTERIZATION OF THE STUDY AREA
The spa tial vari abil ity of en vi ron men tal pa ram e ters, i.e.
physicochemical pa ram e ters of wa ter and geo chem i cal pa ram - e ters of sed i ments, were ana lysed along the depth transect dur - ing each sea son. Fur ther more, the cur rent level of pol lu tion is eval u ated in terms of eutrophication in di ca tors, heavy met als and hy dro car bons dur ing the foraminiferal peak sea son (i.e.
win ter). Pol lu tion pa ram e ters were com pared with the ben thic foraminifera in or der to as sess their ef fects on liv ing as sem - blages. The sa lin ity, tem per a ture, pH, con duc tiv ity, tur bid ity and bi car bon ate al ka lin ity of sea wa ter re sults are pre sented in Ap - pen dix 1. All physicochemical pa ram e ters showed mi nor vari a - tion be tween the sam pling sta tions i.e. sa lin ity 45.6 ± 0.6, tem - per a ture 24.3 ± 3.2°C, pH 8.23 ± 0.04, con duc tiv ity 54656 ± 1777, tur bid ity 0.73 ± 0.01, and bi car bon ate al ka lin ity 103.7 ± 1.1 (Ap pen dix 1). Re sults of grain-size anal y sis doc u -
mented a grad ual de crease of fine sand con tents sea ward foreach sea son (Ap pen dix 1). The TOC ranged from 3379 mg/kg to 10035 mg/kg with the high est value at shal low - est sta tions (Ap pen dix 1).
The en vi ron men tal qual ity of both wa ter and sed i ment was as sessed dur ing the sea son of high est re pro duc tion i.e. win ter in or der to re late to ben thic foraminiferal as sem blages. The level of ni trates and sulphates was high in all sam ples but their con cen tra tion de creased along the transect (Ap pen dix 2).
Com pared to the ER-L (Ef fect Range – Low) and ER-M (Ef fect Range – Me dian) val ues re ported for the United States En vi - ron men tal Pro tec tion Agency’s (USEPA) sed i ment guide lines (Long et al., 1995; Ligero et al., 2002), none of heavy met als were be yond the per mit ted stan dards; how ever, stron tium ex - hib ited higher val ues (Ap pen dix 2). The high est value of hy dro - car bons (9.18 ppm), as THC, was found in the first sta tion and the THC con tent re duced sea ward (Ap pen dix 2). No hy dro car - bons were de tected in sta tions 3, 4 and 5 (Ap pen dix 2).
BENTHIC FORAMINIFERA
All the stud ied sam ples con tained abun dant and well-pre - served liv ing ben thic foraminifera. The foraminiferal den sity var ied be tween 19 and 215 with a mean of 86.4 in di vid u als per 5 cm3. The foraminiferal den sity in creased along the transect and the high est num bers were found at sta tion 5 dur ing all the sea sons (Ap pen dix 3). There was a marked in crease in foraminiferal den sity from sta tions 1 to 4 and then it foraminiferal den sity did not vary con sid er ably be tween sta tions 4 and 5. The high est foraminiferal den sity val ues were found in the win ter sam ples and the low est in the sum mer sam ple (Ap - pen dix 3). The higher value of foraminiferal den sity was mainly due to the in creased num ber of ju ve niles along depth transect in au tumn, win ter and spring whereas, in sum mer, the ju ve nile’s pop u la tion re mained ap prox i mately con stant in all the sta tions (Ap pen dix 3). More spe cif i cally, in the depth transect, the ju ve - niles’ pop u la tion in creased from 58 to 71% dur ing au tumn, 24%
to 49% dur ing win ter, and 21 to 37% dur ing spring. Over all, the ab so lute rel a tive abun dance of ju ve niles was at the high est (65%, on av er age) dur ing au tumn and then re duced to 39% in win ter, 28% in spring, and 27% in sum mer (Ap pen dix 3).
Only six tax o nom i cal groups were found to be liv ing at the mo ment of col lec tion. These were Am mo nia, Glabratellina, Elphidium, Brizalina, miliolids (Cycloforina and Quinque - loculina) and Peneroplidae (Monalysidium, Coscinospira and Peneroplis; Fig. 2). Their ab so lute abun dances along the depth transect and dur ing dif fer ent sea sons are pre sented in Fig ure 3 and Ap pen dix 3. Am mo nia was con sis tently pres ent in all the sta tions dur ing each sea son and dom i nated (39.8%, on av er - age) the ben thic foraminiferal as sem blages (Ap pen dix 3). The sec ond most abun dant group was the miliolids (28.4%, on av er - age) fol lowed by Glabratellina (28.3%, on av er age). Near the fore shore (sta tions 1 and 2), Am mo nia and Glabratellina were the most abun dant taxa, but the rel a tive per cent age of miliolids in creased in the sea ward sta tions (sta tions 3, 4 and 5; cf. Ap - pen dix 3). In con trast, Brizalina sp. was rare and found only dur - ing the spring and au tumn sea sons. Fur ther more, a large num - ber of Am mo nia spec i mens were found dur ing each sea son.
On the ba sis of Shan non’s H’, the low est val ues of di ver sity were doc u mented in sta tion 1 for all sea sons, and lower val ues were found in sum mer. The high est di ver sity val ues were found at sta tions 4 and 5 dur ing win ter; sta tions 3 and 4 dur ing spring;
and sta tions 2 and 3 dur ing au tumn. Dur ing sum mer, the Shan -
non’s H’ val ues are nearly con stant in sta tions 2 and 3 (Fig. 4 and Ap pen dix 3). The dom i nance ranged from 0.31 (3a) to 0.43 (1s), with the high est val ues found in sum mer and close to shore, par tic u larly at sta tion 1 in all sea sons. Re sults of foraminferal con stancy re veal that 100% Am mo nia, Glabratellina and miliolids were found dur ing all sea sons. Con - stancy for Elphidium was 100% in win ter only and re duced to 80% in spring, sum mer and au tumn (Ap pen dix 4). Peneroplidae con stancy was found as 80% dur ing win ter, 40% dur ing spring, 20% dur ing sum mer, and 0% dur ing au tumn. In con trast to these re sults, no liv ing Brizalina spec i mens were found dur ing win ter and sum mer sea sons, how ever, con stancy in creased to 40% in spring and 60% in au tumn (Ap pen dix 4). Rel a tively low val ues (<2%) of foraminiferal al ter ation in dex were doc u - mented.
STATISTICAL ANALYSIS
The clus ter anal y sis re sulted in the group ing of sam ples into two main clus ters (A and B) and two subclusters (A1 and A2) (Fig. 5). Clus ter A rep re sents the near est sta tions to the shore for all sea sons; and clus ter B groups all the off shore sta tions.
Clus ter A has been fur ther sub di vided: clus ter A1, which in - cludes sta tion 1 sam ples from all sea sons, and clus ter A2, which groups to gether mostly sta tions 2 and 3 sta tions of each sea son. Clus ter A1 sam ples are char ac ter ized by the shal low - est wa ter depth, and high est val ues of silt, clay and TOC con - tent. It shows the low est level of foraminiferal den sity and di ver - sity, and the high est level of dom i nance, and in cludes Am mo - nia, Glabratellina, miliolids and Elphidium. Clus ter A2 in cludes sta tions 2 and 3 char ac ter ized by rel a tively lower val ues of TOC com pared to clus ter A1 and in ter me di ate sand con tent. This clus ter is also char ac ter ized by rel a tively higher foraminiferal den sity and sig nif i cant higher val ues of di ver sity com pared with clus ter A1. It also has more abun dant Elphidium and rel a tively less Am mo nia com pared with clus ter A1, the as sem blages of this clus ter also con tains very low per cent ages of Peneroplidae and Brizalina. Clus ter B groups sta tions 4 and 5 from all sea - sons that are deeper and are dom i nated by the low est val ues of fine frac tion and TOC. In terms of ben thic foraminiferal as sem - blages, this clus ter shows the high est val ues of Foraminiferal den sity, and di ver sity and the taxa rep re sent ing it are sim i lar to subcluster A2 in terms of rel a tive abun dance. Fur ther more, clus ter A shows the low est foraminiferal pop u la tion par tic u larly due the low num ber of ju ve niles whereas clus ter B ex hib its the high est foraminiferal den sity and num ber of ju ve niles.
The Q-mode PCA fur ther con firms the rec og ni tion of these groups of sta tions (clus ters and subclusters; Fig. 6). The PCA shows that ~74.0% of the data vari ance can be ex plained by the first two prin ci pal com po nents (fac tors). On the ba sis of Q-mode PCA plan, the first com po nent can be in ter preted as the depth transect (fore shore-off shore gra di ent), whereas the sec ond com po nent might be re lated to the sea son al ity (Fig. 6). More pre cisely, physicochemical pa ram e ters mainly grain-size and sa lin ity are the pre dom i nant el e ments in the first com po nent, while the con tri bu tion to the sec ond com po nent was mainly due to sea son al ity and TOC (Fig. 6). In or der to better un der stand the re la tion ships of bi otic and abiotic data, sec ond ary vari ables (bi otic) were plot ted on the fac tor-planes (Fig. 7). It is clear that foraminiferal den sity and as sem blage in dexes (H’, S, J and E) are linked to the first com po nent, whereas Am mo nia and Glabratellina are re lated though weakly to the sec ond one.
Fig. 2. Scanning electron micrographs of the selected foraminiferal specimens
A – Am mo nia cf. A. parkinsoniana (dor sal view); B – Am mo nia cf. A. parkinsoniana (ven tral view); C – Am mo nia cf. A. parkinsoniana (dor sal view); D – Am mo nia cf. A. parkinsoniana (ven tral view); E – Am mo nia tepida (dor sal view); F – Am mo nia tepida (ven tral view); G– Elphidium excavatum; H – Elphidium advenum; I – Glabratellina sp. 1 (dor sal view); J – Glabratellina sp. 1 (ven tral view); K, M, O – Glabratellina sp. 2 (dor sal views); L, N, P – Glabratellina sp. 2 (ven tral views); Q, R – Quinqueloculina poeyana (lat eral view); S – Quinqueloculina seminula (front view); T – Monalysidium sp. (dor sal view)
Fig. 3. Seasonal variations in the relative abundance of theii six benthic foraminiferal groups
DISCUSSION
In this study, sev eral fac tors in flu enc ing the dis tri bu tion of liv ing foraminiferal as sem blages in the west ern Ara bian Gulf (east ern Bah rain) have been de scribed. These fac tors in clude sea sonal vari a tions of physicochemical pa ram e ters, sed i ment grain-sizes, to tal or ganic car bon, and pol lu tion due to ni trates, sul fates, heavy met als and hy dro car bons. The lo cal ity was ini - tially in ves ti gated by Basson and Murray (1995), who re ported tem po ral vari a tions in four intertidal foraminiferal spe cies (Am - mo nia beccarii, Elphidium advenum, Brizalina pacifica and Nonion sp.) and manly fo cused only on the stand ing crop as - sess ment of the pool. The pres ent study ex tends their find ings in terms of en vi ron men tal char ac ter iza tion as well as sea son al - ity in a sea ward transect. Our re sults show that the high est foraminiferal den sity is found in win ter, which is sim i lar to the find ings of Basson and Murray (1995). The high est foraminiferal den sity might be due to the re pro duc tion of spe - cies of rotaliids and miliolids in early au tumn, which is in di cated
by the pres ence of high ju ve nile num bers. The ef fect of sea son - al ity on stand ing crop has also been re ported by other au thors;
for ex am ple, the high est pop u la tion dur ing win ter was ob served by Basson and Murray (1995) and Korsun and Hald (2000), dur ing spring by Heinz and Hemleben (2003), dur ing spring and sum mer by Ellison (1984), and dur ing spring and au tumn by Fontanier et al. (2003).
Grain-size is known to in flu ence the ben thic foraminiferal as sem blage in terms of di ver sity, den sity, and spe cies com po - si tion (Debenay et al., 2001; Diz et al., 2004; Armynot du Châtelet et al., 2009), which is fur ther con trolled by the hy dro dy - namic re gime of the en vi ron ment (Mo rales et al., 2006). The coarser sed i ments are trans ported and de pos ited by faster-flow ing cur rents than finer sed i ments, which in stead tend to be de pos ited in qui eter wa ters (Tucker, 1995). On the Ara - bian side of the gulf, the seafloor slopes more gently to wards its cen tre than on the Ira nian side and the av er age grain-size in - creases as en ergy in creases (Riegl et al., 2010). In the depth transect, a high per cent age of coarse grains par ti cles in di cate, most prob a bly, the pres ence of faster flow ing cur rents though a Fig. 4. H’ trend in the depth transect during each season
Fig. 5. Dendrogram classification of the stations produced by a Q-mode cluster analysis using the Euclidean distance
Fig. 7. R-mode PCA ordination diagram projecting variables on the factor-planes (1 ´ 2) The secondary variables are marked with a square
Fig. 6. Q-mode PCA ordination diagram plotting samples
The first component can be interpreted as the depth transect (foreshore-offshore gradient), whereas the second component might be related to the seasonality
pos si ble pro duc tion of biogenic grains as in car bon ate en vi ron - ments can not be ex cluded. How ever, the pres ence of fine grain sed i ments in the sta tions close to shore line could be due to low en ergy con di tions in the shal low-wa ter en vi ron ment. Liv ing foraminifera, par tic u larly ju ve niles, were more com monly found in sam ples with higher coarse sand con tent. The pos i tive re la - tion ship be tween ju ve niles’ pop u la tion and sed i ment grain-size might sug gest that coarse-grained sed i ments may better sup - port the re pro duc tion of ga metes and the sur vival of ju ve niles when com pared with fine-grained sed i ments. Coarse-grained sed i ments also of fer fa vour able con di tions to ben thic foraminifera in terms of pro vid ing hab i tat to the flora (e.g., microalgae and bac te rial films) that ul ti mately pro vides food/nu - tri ents to the liv ing pop u la tion (Loubere and Fariduddin, 1999;
Ward et al., 2003; Diz et al., 2004; Top ping et al., 2006). Lastly, high in er tia of the first prin ci ple com po nent (i.e. par ti cle grain-size) agrees with Murray’s niche the ory, which states that the dis tri bu tions pat terns of ben thic foraminifera are con trolled by en vi ron men tal fac tors (reach ing crit i cal thresh olds alone or in com bi na tion; Murray, 2001).
An other rea son for the lower pop u la tion of ju ve niles near the fore shore seems to be due to the pres ence of al gal mat. Our anal y ses sug gest that the site might be in flu enced by eutrophication par tic u larly by el e vated ni trates and sulphates, and the al gal mat spread ing along the beach at shal low-wa ter depth might sup port it. The pres ence of al gal mat may hin der adults to re pro duce and re sult in a de crease in foraminiferal den sity near the fore shore (Rich ard son, 2006). In the off shore di rec tion, al gal growth di min ishes as wa ter depth in creases, which re sults in more fa vour able con di tions for foraminifera. In - creas ing foraminiferal den sity in an off shore di rec tion dur ing an eutrophication event has also been re ported in ear lier stud ies (Rich ard son, 2006; Nardelli et al., 2010). Higher TOC con tent in nearshore sta tions 1 and 2 could be due to the high pri mary pro - duc tiv ity of al gae. How ever, the over all TOC con tent de creased along the transect as coarser sed i ments al low less TOC to ac - cu mu late com pared to finer sed i ments (Mar tins et al., 2011).
The high est lev els of TOC were found in win ter and au tumn, dou ble the con tent of the other two sea sons. The high est foraminiferal den sity oc curred in win ter. Slight vari a tions among physicochemical pa ram e ters were re corded for the depth transect dur ing each sea son. These mi nor vari a tions could be due to the mix ing be tween bot tom and sur face wa ter in the shal - low coastal ar eas. How ever, this in te grated per spec tive may pro vide an un der stand ing of the fac tors in flu enc ing pop u la tion dy nam ics as a whole rather a de creas ing or in creas ing pro file along the transect in each sea son (Albani et al., 1984).
In ad di tion to the foraminiferal den sity, di ver sity in the depth transect var ied due to changes in en vi ron men tal pa ram e ters.
Of the six groups of liv ing foraminifera found in the depth transect, Am mo nia and Glabratellina were found to be dom i - nant in each sea son, miliolids were dom i nant only in win ter and spring, and Elphidium, Peneroplidae and Brizalina were never dom i nant (Dom i nant: re fers to >20% in rel a tive abun dance).
More spe cif i cally, the spe cies struc ture for each group was as fol lows: one spe cies of Am mo nia (Am mo nia sp. 1 cf. A.
parkinsoniana), two spe cies of Glabratellina (Glabratellina sp. 1 and sp. 2), one spe cies of Elphidium (Elphidium advenum), one spe cies of Brizalina (Brizalina pacifica), three spe cies of miliolids (Quinqueloculina seminula, Quinqueloculina poeyana, and Quinqueloculina sp. 1), and three spe cies of peneroplids (Monalysidium sp. 1, Coscinospira sp. 1 and Peneroplis pertusus). Pre vi ously, in the same lo cal ity but from the pool, Basson and Murray (1995) re ported the tem po ral vari a tion of four spe cies, i.e. Am mo nia beccarii, Elphidium advenum, Nonion sp., and Brizalina pacifica; how ever, no Glabratellina,
miliolids or peneroplids were re ported. In con trast, Nonion sp.
was not found in the pres ent study. Ear lier stud ies have also re - ported dif fer ent spe cies of Am mo nia, Elphidium, and miliolids in the shal low-wa ter en vi ron ment of the Ara bian Gulf, how ever, Glabratellina has not been re corded (Cherif et al., 1997;
Al-Enezi and Frontalini, 2015; Parker and Gischler, 2015).
Foraminiferal con stancy re vealed that both Am mo nia and Glabratellina were con sis tently pres ent along the transect, ir re - spec tive of sed i ment grain-size and sea sonal vari a tions. This sup ports the find ing that some rotaliids might be ca pa ble of re - pro duc ing rap idly in many dif fer ent en vi ron ments (Alve, 1995).
For in stance, Am mo nia tepida has been re ported as an op por - tu nis tic spe cies along the Med i ter ra nean coast in the vi cin ity of a sew age sludge dis posal site and other sources of pol lu tion (Frontalini et al., 2009, 2013; Hyams-Kaphzan et al., 2009). In con trast, miliolids were less abun dant near the fore shore (1st and 2nd sta tions), but their rel a tive abun dance in creased in the off shore di rec tion. This could be due to the fact that miliolids were af fected by eutrophy, how ever, their rel a tive per cent age in creased with de crease in the pol lut ants con cen tra tion along the depth transect (Ap pen dix 1; Figs. 3 and 7). Sim i larly, the rel - a tive abun dance of Elphidium in creased along the depth transect which could be due to their high af fin ity with coarse sand par ti cles. On the con trary, Glabratellina were con sis tently pres ent along the transect ir re spec tive of the sea sonal vari a - tions and grain-size; how ever, no ear lier re ports are avail able on their dis tri bu tional pat terns in shal low-wa ter en vi ron ments.
Com par a tively, both Elphidium and Glabratellina showed higher abun dance in win ter and low est in sum mer but their over all in creased in the sea ward di rec tion. Lastly, Brizalina are found only twice, in spring and au tumn. They are found in the fine to me dium grain sub strate com pared to very fine or coarse grain en vi ron ments. Debenay et al. (2001) cor re lated the pres - ence of this ge nus with fine-grained sed i ments.
Among sed i ment grain-size, it can be es tab lished that coarse and me dium sand par ti cles al low the ma jor ity of the ju - ve nile pop u la tion to sur vive and re pro duce suc cess fully com - pared with the clay and fine sand. Clay and fine sand better sup ported the adult pop u la tion. Sim i larly, the higher con cen tra - tion of ni trates and sulphates near the fore shore can be seen to af fect the pop u la tion at these sta tions (Schafer, 1973). The el e - men tal anal y sis and their com par i son with de vised lev els in di - cated that the area is not af fected by heavy metal pol lu tion ex - cept stron tium when com pared with other parts of the world (Turekian, 1964; Holmes, 1973; Milliman et al., 2012). The el e - vated stron tium could be due its af fin ity with gyp sum and other car bon ates which are abun dant in the Ara bian Gulf (But ler, 1969; Ev ans, 1995). The over all foraminiferal al ter ation in dex was <2%, which sup ports the find ing that the area is un pol luted.
Sim i larly, the ab sence of THC pol lu tion fur ther con firms that the site is not af fected by hy dro car bons, and can be con sid ered as ref er ence sta tion for fu ture stud ies.
CONCLUSIONS
We re corded the abun dance, di ver sity, and as sem blage com po si tion of ben thic foraminifera along a depth transect in east ern Bah rain. We ob served pro nounced sea son al ity in the ben thic foraminiferal pop u la tions. The high est stand ing crop was ob served in win ter, while the high est pro por tion of ju ve niles was found in au tumn. The pro por tion of ju ve niles along the transect in creased in the off shore di rec tion. Anal y sis of heavy met als, hy dro car bons, and nu tri ents in di cated that the stud ied site is not pol luted, and there fore pro vides base line in for ma tion for fu ture stud ies re lated to pol lu tion.
Ac knowl edge ments. Fund ing for this pro ject was pro vided by the Dean ship of Sci en tific Re search, King Fahd Uni ver sity of Pe tro leum and Min er als, un der grant IN121028. We thank E. Setoyama and A. Amao for help with sam ple col lec tion,
K. Al-Ramadan for ad vice and lo gis ti cal sup port, M. Holzmann for SEM pho tog ra phy, and J. Parker for ad vice on the tax on omy of the ben thic foraminifera. The au thors grate fully ac knowl edge Dr. J. Parker and Dr. F. Fiorini for their con struc tive com ments that greatly im proved the manu script.
REFERENCES
Albani, A.D., Favero, V., Barbero, R.S., 1984. Benthonic foraminifera as in di ca tors of intertidal en vi ron ments. Geo-ma - rine Let ters, 4: 43–47.
Al-Enezi, E., Frontalini, F., 2015. Ben thic foraminifera and en vi ron - men tal qual ity: the case study of Sulaibikhat Bay (Ku wait). Ara - bian Jour nal of Geosciences, 8: 1–12.
Alve, E., 1995. Ben thic foraminiferal re sponses to estuarine pol lu - tion: a re view. Jour nal of Foraminiferal Re search, 25: 190–203.
Amao, A., 2014. Find ing John Murray’s “Warm Shal low Pool” in Bah rain. News let ter of Micropalaeontology, 89: 70–71.
Armynot du Châtelet, É., Debenay, J.-P., 2010. The anthropogenic im pact on the west ern French coasts as re vealed by foraminifera: a re view. Re vue de Micropaléontologie, 53:
129–137.
Armynot du Châtelet, É., Bout-Roumazeilles, V., Riboulleau, A., Trentesaux, A., 2009. Sed i ment (grain size and clay min er al - ogy) and or ganic mat ter qual ity con trol on liv ing ben thic foraminifera. Re vue de Micropaléontologie, 52: 75–84.
ASTM, C., 1984. Stan dard Test Method for Sieve Anal y sis of Fine and Coarse Ag gre gates.
Basson, P.W., Murray, J.W., 1995. Tem po ral vari a tions in four spe - cies of intertidal foraminifera, Bah rain, Ara bian Gulf.
Micropaleontology, 41: 69–76.
Basson, P.W., Mohamed, S.A., Arora, D.K., 1989. A sur vey of the ben thic ma rine al gae of Bah rain. Botanica Ma rina, 32: 27–40.
Burt, J.A., 2014. The en vi ron men tal costs of coastal ur ban iza tion in the Ara bian Gulf. City: anal y sis of ur ban trends, cul ture, the ory, pol icy, ac tion, 18: 760–770.
But ler, G.P., 1969. Mod ern evaporite de po si tion and geo chem is try of co ex ist ing brines, the sabkha, Trucial Coast, Ara bian Gulf.
Jour nal of Sed i men tary Re search, 39: 70–89.
Cherif, O.H., Al-Ghadban, A.-N., Al-Rifaiy, I.A., 1997. Dis tri bu tion of foraminifera in the Ara bian Gulf. Micropaleontology, 43:
253–280.
Coles, S.L., McCain, J.C., 1990. En vi ron men tal fac tors af fect ing ben thic infaunal com mu ni ties of the West ern Ara bian gulf. Ma - rine En vi ron men tal Re search, 29: 289–315.
Debenay, J.-P., Tsakiridis, E., Soulard, R., Grossel, H., 2001.
Fac tors de ter min ing the dis tri bu tion of foraminiferal as sem - blages in Port Joinville Har bor (Ile d’Yeu, France): the in flu ence of pol lu tion. Ma rine Micropaleontology, 43: 75–118.
Diz, P., Francés, G., Costas, S., Souto, C., Alejo, I., 2004. Dis tri bu - tion of ben thic foraminifera in coarse sed i ments, Ría de Vigo, NW Ibe rian mar gin. Jour nal of Foraminiferal Re search, 34:
258–275.
Ellison, R., 1984. Foraminifera and meiofauna on an intertidal mud - flat, Cornwall, Eng land: pop u la tions, res pi ra tion and sec ond ary pro duc tion, and en ergy bud get. Hydrobiologia, 109: 131–148.
Ev ans, G., 1995. The Ara bian Gulf: a mod ern car bon ate-evaporite fac tory: a re view. Cuadernos de Geología Ibérica, 19: 61–98.
Frontalini, F., Coccioni, R., 2011. Ben thic foraminifera as bioindicators of pol lu tion: a re view of Ital ian re search over the last three de cades. Re vue de Micropaléontologie, 54: 115–127.
Frontalini, F., Buosi, C., Da Pelo, S., Coccioni, R., Cherchi, A., Bucci, C., 2009. Ben thic foraminifera as bio-in di ca tors of trace el e ment pol lu tion in the heavily con tam i nated Santa Gilla la - goon (Cagliari, It aly). Ma rine Pol lu tion Bul le tin, 58: 858–877.
Frontalini, F., Margaritelli, G., Francescangeli, F., Rettori, R., Châtelet, E.A. du, Coccioni, R., 2013. Ben thic foraminiferal as - sem blages and biotopes in a coastal lake: the case study of Lake Varano (south ern It aly). Acta Protozoologica, 52:
147–168.
Fontanier, C., Jorissen, F.J., Chaillou, G., Da vid, C., Anschutz, P., Lafon, V., 2003. Sea sonal and interannual vari abil ity of ben - thic foraminiferal fau nas at 550 m depth in the Bay of Biscay.
Deep Sea Re search Part I: Ocean o graphic Re search Pa pers, 50: 457–494.
Haake, F.W., 1970. Zur Tiefenverteilung von Miliolinen (Foram.) im Persischen Golf. Paläontologische Zeitschrift, 44: 196–200.
Hamza, W., Munawar, M., 2009. Pro tect ing and man ag ing the Ara - bian Gulf: past, pres ent and fu ture. Aquatic Eco sys tem Health &
Man age ment, 12: 429–439.
Hay ward, B.W., Holzmann, M., Grenfell, H.R., Pawlowski, J., Triggs, C.M., 2004. Mor pho log i cal dis tinc tion of mo lec u lar types in Am mo nia-to wards a tax o nomic re vi sion of the world’s most com monly mis iden ti fied foraminifera. Ma rine Micropaleon - tology, 50: 237–271.
Heinz, P., Hemleben, C., 2003. Re gional and sea sonal vari a tions of re cent ben thic deep-sea foraminifera in the Ara bian Sea. Deep Sea Re search Part I: Ocean o graphic Re search Pa pers, 50:
435–447.
Holmes, C.W., 1973. Dis tri bu tion of se lected el e ments in surficial ma rine sed i ments of the north ern Gulf of Mex ico con ti nen tal shelf and slope. US Govt. Print. Off.
Hottinger, L., Halicz, E., Reiss, Z., Drobne, K., 1993. Re cent Foraminiferida from the Gulf of Aqaba, Red Sea. Dela, Slovenska Akademija Znanosti in Umetnosti, 33: 179–230.
Hyams-Kaphzan, O., Almogi-Labin, A., Benjamini, C., Herut, B., 2009. Nat u ral oligotrophy vs. pol lu tion-in duced eutrophy on the SE Med i ter ra nean shal low shelf (Is rael): en vi ron men tal pa ram e - ters and ben thic foraminifera. Ma rine Pol lu tion Bul le tin, 58:
1888–1902.
John, V., Coles, S., Abozed, A., 1990. Sea sonal cy cles of tem per a - ture, sa lin ity and wa ter masses of the west ern Ara bian Gulf.
Oceanologica Acta, 13: 273–281.
Korsun, S., Hald, M., 2000. Sea sonal dy nam ics of ben thic foraminifera in a gla cially fed fjord of Svalbard, Eu ro pean Arc tic.
Jour nal of Foraminiferal Re search 30: 251–271.
Ligero, R. A., Barrera, M., Casas-Ruiz, M., Sales, D., Lopez-Aguayo, F., 2002. Dat ing of ma rine sed i ments and time evo lu tion of heavy metal con cen tra tions in the Bay of Cádiz, Spain. En vi ron men tal Pol lu tion, 118: 97–108.
Loeblich, A.R., Tappan, H.N., 1994. Foraminifera of the Sahul shelf and Timor Sea. Cushman Foun da tion for Foraminiferal Re - search Spe cial Pub li ca tion, 31: 51, 142, 165, 166, 168.
Long, E.R., Mac Don ald, D.D., Smith, S.L., Cal der, F.D., 1995. In ci - dence of ad verse bi o log i cal ef fects within ranges of chem i cal con cen tra tions in ma rine and estuarine sed i ments. En vi ron - men tal Man age ment, 19: 81–97.
Loubere, P., Fariduddin, M., 1999. Ben thic Foraminifera and the flux of or ganic car bon to the sea bed. In: Mod ern Foraminifera (ed. B.K. Sen Gupta): 181–199. Kluwer Ac a demic Pub lish ers, Lon don.
Lutze, G.F., 1974. Benthische Foraminiferen in Oberfläschen-Sedi - menten des Persischen Golfes, Teil, 1: 1–66.
Mar tins, V., Yamashita, C., Sousa, S.H.M., Mar tins, P., Laut, L.L.M., Figueira, R.C.L., Mahiques, M.M., Ferreira da Silva, E., Rocha, F., Dias, J.M.A., 2011. The re sponse of ben thic foraminifera to pol lu tion and en vi ron men tal stress in Ria de Aveiro (N Por tu gal). Jour nal of Ibe rian Ge ol ogy, 37: 231–243.
Milliman, J., Müller, G., Förstner, F., 2012. Re cent Sed i men tary Car bon ates: Part 1 Ma rine Car bon ates. Springer, Berlin-Hei del - berg.
Mo rales, J.A., Delgado, I., Gutierrez-Mas, J.M., 2006. Sed i men - tary char ac ter iza tion of bed types along the Guadiana es tu ary (SW Eu rope) be fore the con struc tion of the Alqueva dam.
Estuarine Coastal and Shelf Sci ence, 70: 117–131.
Murray, J.W., 1965a. The Foraminiferida of the Per sian Gulf. Part 1.
Rosalina adhaerens sp. nov. An nals and Mag a zine of Nat u ral His tory, 8: 77–79.
Murray, J.W., 1965b. The Foraminiferida of the Per sian Gulf. Part 2.
The Abu Dhabi re gion. Palaeo ge ogra phy, Palaeoclimatology, Palaeo ec ol ogy, 1: 307–332.
Murray, J.W., 1966a. The Foraminiferida of the Per sian Gulf. Part 6.
Liv ing forms in the Abu Dhabi re gion. Jour nal of Nat u ral His tory, 4: 55–67.
Murray, J.W., 1966b. The Foraminiferida of the Per sian Gulf. Part 3.
The Halat al Bahrani re gion. Palaeo ge ogra phy, Palaeoclima - tology, Palaeo ec ol ogy, 2: 59–68.
Murray, J.W., 1966c. The Foraminiferida of the Per sian Gulf. Part 4.
Khor al Bazam. Palaeo ge ogra phy, Palaeoclimatology, Palaeo - ec ol ogy, 2: 153–169.
Murray, J.W., 1966d. The Foraminiferida of the Per sian Gulf. Part 5.
Palaeo ge ogra phy, Palaeoclimatology, Palaeo ec ol ogy, 2:
267–278.
Murray, J.W., 1991. Ecol ogy and Palaeo ec ol ogy of Ben thic Foraminifera. Longman Sci en tific & Tech ni cal, New York.
Murray, J.W., 2001. The niche of ben thic foraminifera, crit i cal thresh olds and prox ies. Ma rine Micropaleontology, 41: 1-7.
Murray, J.W., 2006. Ecol ogy and Ap pli ca tions of Ben thic Foraminifera. Cam bridge Uni ver sity Press.
Murray, J.W., Alve, E., 2002. Ben thic foraminifera as in di ca tors of en vi ron men tal change: mar ginal-ma rine, shelf and up per-slope en vi ron ments. In: Qua ter nary En vi ron men tal Micropalaeonto - logy (ed. S.K. Haslett): 59–90. Ed ward Ar nold (Pub lish ers) Lim - ited, Lon don.
Nardelli, M., Jorissen, F., Pusceddu, A., Morigi, C., Dell’Anno, A., Danovaro, R., De Stigter, H.C., Negri, A., 2010. Liv ing ben thic foraminiferal as sem blages along a lat i tu di nal transect at 1000m depth off the Por tu guese mar gin. Micropaleontology, 56:
323–344.
Oostdam, B.L., 1980. Oil pol lu tion in the Per sian Gulf and ap - proaches, 1978. Ma rine Pol lu tion Bul le tin, 11: 138144.
Ortiz, J.D., Mix, A.C., Col lier, R.W., 1995. En vi ron men tal con trol of liv ing sym bi otic and asymbiotic foraminifera of the Cal i for nia Cur rent. Paleoceanography, 10: 987–1009.
Parker, W.C., Ar nold, A.J., 2000. Quan ti ta tive meth ods of data anal y sis in foraminiferal ecol ogy. In: Mod ern Foraminifera (ed.
B.K. Sen Gupta): 71–89. Kluwer Ac a demic Pub lisher, Dordrecht.
Parker, J.H., Gischler, E., 2015. Mod ern and rel ict foraminiferal biofacies from a car bon ate ramp, off shore Ku wait, north west Per sian Gulf. Fa cies, 61: 1–22.
Paul, B., Bar ren, L., Nesterenko, P., 2005. The de ter mi na tion of phos phates in en vi ron men tal sam ples by ion chro ma tog ra phy.
In: Chro mato graphic Anal y sis of the En vi ron ment (ed. L.M.L.
Nollet): 263–286. The Chem i cal Rub ber Com pany (CRC) Press.
Riegl, B., Poiriez, A., Janson, X., Berg man, K.L., 2010. The gulf:
fa cies belts, phys i cal, chem i cal, and bi o log i cal pa ram e ters of sed i men ta tion on a car bon ate ramp. In: Car bon ate Depositional Sys tems: As sess ing Di men sions and Con trol ling Pa ram e ters (eds. H. Westphal, B. Riegl and G.P. Eberli): 145–213. Springer, Neth er lands.
Rich ard son, S.L., 2006. Re sponse of epiphytic foraminiferal com - mu ni ties to nat u ral eutrophication in sea grass hab i tats off Man O’War Cay, Belize. Ma rine Ecol ogy, 27: 404–416.
Samir, A.M., Abdou, H.F., Zazou, S. M., El-Menhawey, W.H.,2003.
Clus ter anal y sis of re cent ben thic foraminifera from the north - west ern Med i ter ra nean coast of Egypt. Re vue de Micropa - leonto logie, 46: 111–130.
Sarita, C., Delminda, M., Si mon, C., Da vid, S., Tomasz, B., 2015.
Eco log i cal zonation of ben thic foraminifera in the lower Guadiana Es tu ary (south east ern Por tu gal). Ma rine Micropaleontology, 114: 1–18.
Schafer, C.T., 1973. Dis tri bu tion of foraminifera near pol lu tion sources in Chaleur Bay. Wa ter, Air, and Soil Pol lu tion, 2:
219–233.
Scott, D.B., Schafer, C.T., Honig, C., Youn ger, D.C., 1995. Tem po - ral vari a tions of ben thic foraminiferal as sem blages un der or near aquaculture op er a tions; doc u men ta tion of im pact his tory.
Jour nal of Foraminiferal Re search, 25: 224–235.
Shan non, C.E., 1948. A math e mat i cal the ory of com mu ni ca tion.
Bell Sys tem Tech ni cal Jour nal, 27: 379–423.
Shan non, C.E., Weaver, W., 1963. The Math e mat i cal The ory of Com mu ni ca tion. Uni ver sity of Il li nois Press, Ur bana.
Top ping, J.N., Murray, J.W., Pond, D.W., 2006. Sew age ef fects on the food sources and diet of ben thic foraminifera liv ing in oxic sed i ment: a mi cro cosm ex per i ment. Jour nal of Ex per i men tal Ma rine Bi ol ogy and Ecol ogy, 329: 239–250.
Tucker, M., 1995. The Field De scrip tion of Sed i men tary Rocks.
Geo log i cal So ci ety of Lon don Hand book, John Wiley & Sons.
Turekian, K.K., 1964. The ma rine geo chem is try of stron tium.
Geochimica et Cosmochimica Acta, 28: 1479–1496.
Ward, J.N., Pond, D.W., Murray, J.W., 2003. Feed ing of ben thic foraminifera on di a toms and sew age-de rived or ganic mat ter: an ex per i men tal ap pli ca tion of lipid biomarker tech niques. Ma rine En vi ron men tal Re search, 56: 515–530.
Wil son, M.B., Zhang, C.C., Gan dhi, J., 2011. Anal y sis of in or ganic ni tro gen and re lated an ions in high sa lin ity wa ter us ing ion chro - ma tog ra phy with tan dem UV and con duc tiv ity de tec tors. Jour nal of Chro mato graphic Sci ence, 49: 596–602.
Yanko, V., Ahmad, M. Kaminski, M.A., 1998. Mor pho log i cal de for - mi ties of ben thic foraminiferal tests in re sponse to pol lu tion by heavy met als: im pli ca tions for pol lu tion mon i tor ing. Jour nal of Foraminiferal Re search, 28: 177–200.
