Dinoflagellate cyst distribution in the oligotrophic environments of the Gulf of Aqaba and northern Red Sea

Marine Micropaleontology 124 (2016) 29–44

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Research paper

Dinoflagellate cyst distribution in the oligotrophic environments of the Gulf of Aqaba and northern Red Sea Rehab Elshanawany a,b, Karin A.F. Zonneveld a,c,⁎ a b c

MARUM, Leobener Straße, University of Bremen, D-28359 Bremen, Germany Faculty of Science, Baghdad St., Moharam Bey 21511, Alexandria University, Egypt Fachbereich 5-Geowissenschaften, University of Bremen, Postfach 330440, D-28334 Bremen, Germany

a r t i c l e

i n f o

Article history: Received 29 July 2014 Received in revised form 15 January 2016 Accepted 17 January 2016 Available online 20 January 2016 Keywords: Dinoflagellate cysts Gulf of Aqaba Northern Red Sea Oligotrophic environment

a b s t r a c t Oligotrophic environmental systems form a major part of the marine aquatic environments on earth. Compared to mesotrophic and eutrophic environments extremely little information is available about the relationship between the distribution of organic-walled dinoflagellate cysts and physical and biological gradients in the upper water column. Here we present the first comprehensive study of the modern geographic distribution of organic-walled dinoflagellate cysts in the oligotrophic environments of the northern Red Sea and Gulf of Aqaba. We show that sediments of both regions have characteristic dinoflagellate cyst associations consisting of both heterotrophic and phototrophic species of which the latter, including both autotrophic and mixotrophic species, form the major part of the associations in both regions. The upper water environment of the Gulf of Aqaba is characterized by slightly enhanced nutrient concentrations compared to the Red Sea, due to water column mixing in winter. Its phytoplankton composition is dominated by pico- and ultra-plankton and a slight higher amount of eukaryotes compared to northern Red Sea. Its sedimentary cyst associations are characterized by higher relative and absolute abundances of the species Brigantedinium spp., Votadinium calvum, Echinidinium spp., Lingulodinium machaerophorum, Spiniferites spp., Spiniferites bentorii, Spiniferites membranaceus and Spiniferites mirabilis. Sediments of the northern Red Sea are characterized by high relative abundances of Impagidinium aculeatum, Impagidinium sphaericum, Operculodinium israelianum, Operculodinium longispinigerum, Operculodinium centrocarpum, cysts of Pentapharsodinium dalei, and Selenopemphix nephroides. A positive relationship between the distribution of the heterotrophic species Brigantedinium spp., Echinidinium spp. and V. calvum with the occurrence of other eukaryotic groups such as e.g. diatoms is documented. The distribution of S. nephroides cannot be related to the presence of diatom occurrences and it is suggested that the distribution of food sources other than diatoms affects its distribution. We document a positive relationship between the sedimentary distribution of the phototrophic dinoflagellate species L. machaerophorum and Spiniferites species and the abundance of the cyanobacteria Synechococcus in the water column. Since Synechococcus is known to be a potential prey of Lingulodinium polyedrum and members of the Gonyaulax spinifera complex (the motile forms producing these cysts) we suggest a possible cyst distribution–prey relationship of mixotrophic dinoflagellates. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Marine dinoflagellates are motile eukaryotic single cell organisms that constitute one of the major groups of marine plankton (e.g. Gómez, 2005; Bravo and Figueroa, 2014). They play a central role in the marine planktic food web and can have autototrophic, heterotrophic and mixotrophic life strategies (e.g. Ignatiades, 2012). There are more than 2000 extant dinoflagellate species (Taylor et al., 2008), about half ⁎ Corresponding author at: MARUM, Leobener Straße, University of Bremen, D-28359 Bremen, Germany. E-mail address: [email protected] (R. Elshanawany).

http://dx.doi.org/10.1016/j.marmicro.2016.01.003 0377-8398/© 2016 Elsevier B.V. All rights reserved.

of them are autotrophic and as such, they directly contribute to primary production. During reproduction, several dinoflagellate species can produce cysts that have a high potential to become fossilized in the sediments (Zonneveld et al., 2008). Dinoflagellates inhabit surface waters in a wide range of marine environments. The abundance and distribution of their cysts depend upon environmental parameters such as sea-surface temperature (SST), seasurface salinity (SSS), micro and macro nutrient availability, sea ice cover, bottom water oxygen concentrations and prey distribution (e.g. de Vernal et al., 2001, 2005; Pospelova et al., 2004, 2008; Holzwarth et al., 2007; Radi et al., 2007; Radi and de Vernal, 2008; Zonneveld et al., 2008, 2010; Bouimetarhan et al., 2008; Elshanawany et al.,

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R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44

2010; Heikkilä et al., 2014). The sedimentary cyst associations form natural archives that can be used to reconstruct upper water environmental conditions at times of deposition and they have proven to be extremely useful as tracers of upper water productivity changes related to changes in the trophic state of upper waters (e.g. due to pollution related to human activities such as urbanization and industrialization, Dale and Fjellså, 1994; Dale, 1996; Pospelova et al., 2002; Krepakevich and Pospelova, 2010; Satta et al., 2010; Shin et al., 2010a, 2010b; Zonneveld et al., 2012). In many palaeo-environmental studies, the occurrence of high relative concentrations of cysts produced by heterotrophic species in the sediments is used as an indicator that eutrophic conditions might have prevailed at times of sediment deposition whereas high concentrations of phototrophic dinoflagellates are used to infer low productive conditions (e.g. Kumar and Patterson, 2002; Vasquez-Bedoya et al., 2008; Houben et al., 2013, and references therein). This is based on the assumption that heterotrophic dinoflagellates, that graze on a wide array of primary producers such as bacteria, nanoflagellates, hapto- and prasinophytes, other dinoflagellates and notably diatoms (Jeong et al., 2008, 2010) increase their cyst production when more food is available. In turn, increased availability in macro and/or micronutrients results in increased primary productivity and as such increased prey availability. However during the last decades it has become clear that the sedimentary dinocyst eutrophication signal is not that straightforward and differs in different regions depending on the local oceanographic and other environmental conditions. Dale (2009) suggested two main changes in the sedimentary dinoflagellate cyst association as a result of eutrophication of upper waters: a. the so called “Oslo-Fjord signal” and b. the “heterotrophic signal”. The first describes an increase in concentrations of the photosynthetic species of which Lingulodinium machaerophorum often accounts for most of the increase. The second effect is an increase in absolute and/or relative amount of cysts formed by heterotrophic dinoflagellate species. The latter as being a result of either proportional increase in production of heterotrophic cysts or a proportional decrease of cysts formed by phototrophic species e.g. as a result of light inhibition. The first signal is confirmed in later studies for several regions such as fjords, river systems, and bays (e.g. Shin et al., 2010b; Zonneveld et al., 2012). In regions characterized by seasonally or temporarily stratified upper waters such as the Po-river system and Hudson Bay system, the phototrophic species cyst of Pentapharsodinium dalei becomes highly abundant with higher trophic levels (e.g. Zonneveld et al., 2012; Heikkilä et al., 2014). In other regions, it is observed that heterorotrophic cysts, notably Polykrikos, Stelladinium stellatum and Brigantedinium species exhibit increased cyst production or relative abundance in responds to (anthropogenic) eutrophication (Sætre et al., 1997; Kim et al., 2009; Pospelova and Kim, 2010; Shin et al., 2010b; Zonneveld et al., 2012). Moreover, Diplopsalidaceae, such as Dubridinium spp. are typical indicators of anthropogenic eutrophication in some coastal areas (e.g. Pospelova et al., 2002; Pospelova and Kim, 2010). To be able to determine eutrophication in downcore records it is important to have detailed information about the cyst signal characteristic for pre-eutrophication conditions. Unfortunately only extremely limited information is available about the relationship between cyst distribution and environmental settings in oligotrophic environments. In this study, we focus on the extreme oligotrohic environmental ecosystems of the northern Red Sea and Gulf of Aqaba (Figs. 1, 2). To date only two studies on the dinoflagellate cyst assemblages are available for the central Red Sea whereas studies on the northern part of this basin and the Gulf of Aqaba are absent (Wall and Warren, 1969; Mohamed and Al-Shehri, 2011). Wall and Warren (1969) studied the change in dinoflagellate cyst association in low temporal resolution during the last four glacial–interglacial cycles in two cores from the southern central region of the Red Sea. They related the distribution of dinoflagellate cysts in the cores to changing conditions of temperature, salinity and sea level and referred to four glacial cycles, were they have

been recognized from oxygen isotope studies. However, in the late 1960s, only a limited amount of the presently known species were described and consequently, in this study only a part of the cyst association has been documented. Furthermore, at that time, it was not possible to establish a detailed stratigraphy of the cores, nor was it possible to obtain quantitative reconstructions of the environmental hampering the establishment of a relationship between cyst occurrences and environmental parameters. In a more recent study, Mohamed and AlShehri (2011) focus on the germination of dinoflagellate cysts collected from surface sediments at six locations along the southwestern Red Sea coast of Saudi Arabia. These authors however do not provide information about the complete cyst association nor the relationship between cyst distribution and environmental conditions of the surface waters. During the last decades it has become clear that many if not all phototrophic dinoflagelates are mixotrophic and dependent in some part of their life cycle on the ingestion of prey (e.g. Taylor et al., 2008; Hoppenrath et al., 2009; Jeong et al., 2010). It can be hypothesized that the distribution of mixotrophic dinoflagellates is dependent on the distribution of their prey as well. To date this aspect has not been investigated. Here we will provide the first comprehensive cyst distribution study from two extreme oligotrophic environmental systems where concentrations of major inorganic nutrients are often below the detection limit (Berninger and Wickham, 2005 and references therein). We provide detailed information about the relationship between the geographic sedimentary cyst distribution and upper ocean environmental conditions as well as the composition and characteristics of the microbial community. We will show that the cyst distribution of both phototrophic as well as heterotrophic dinoflagellate cysts can be related to the distribution of their potential prey. 2. Environmental setting The Red Sea is a narrow oceanic basin separating northern Africa from the Arabian subcontinent. It is landlocked at three sides. Its northern part extends to about 30° N and is formed by two side basins; the Gulf of Suez and the Gulf of Aqaba. In the south it is connected to the Arabian Sea through the strait of Bab el Mandab and Gulf of Aden at approximately 12.5° N (Fig. 1). The Gulf of Aqaba, is the side arm of the Red Sea that forms the eastern border to the Sinai Peninsula. It is a 180 kmlong, deep (max. depth 1820 m), narrow basin (2–25 km wide), with no pronounced shelf region. It is separated from the Red Sea by a shallow sill (max. depth 242 m), the Strait of Tiran (Fig. 2). The Red Sea and Gulf of Aqaba have no river discharge. This leads, combined with the extremely scant rainfall and high evaporation rates, in a negative water balance leading to stratified upper water column conditions with very high salinity concentrations of ≥40.5 (Table 1, Weisse, 1989). Both basins are characterized by stable surface water eddies that have an anti-clockwise direction (Figs. 1, 2, Sofianos and Johns, 2003; Afargan and Gildor, 2015). In winter a northward flowing coastal surface current can be observed along the eastern Red Sea, this current is reversed in summer where it has a southward direction. Sea-surface temperatures are high throughout the year ranging from about 30.5 °C in summer to 22.5 in winter (Raitsos et al., 2013). Being surrounded by desert there is no allochthonous nutrient input resulting in extreme oligotrophic conditions and low phytoplankton productivity in both basins (Fig. 1, Table 1). Nitrate concentrations in the photic zone of in the Gulf of Aqaba vary between about 0.01 to 1.20 μM in summer and winter, respectively, whereas Phosphate concentrations vary between 0.01–0.13 μM in summer and winter respectively (Badran, 2001). Exception is formed in the most northern tip of the Gulf of Aqaba where local pollution is reflected in nitrate concentrations measured in the water column in late winter/early spring 1999 (Berninger and Wickham, 2005). No difference in concentrations of Silicate and Phosphate could be detected though.

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Fig. 1. Map of the research area depicting upper water chlorophyll-a concentrations and sample positions (redrawn using google-earth maps, version 2014).

In contrast to the Red Sea, the Gulf of Aqaba is not stratified throughout the whole year. Due to winter cooling and very high evaporation rates, a vertical mixing of the water column can occur down to 900 m depth (Genin et al., 1995). During this time deep waters are produced that flow southward over the sill through the Stait of Tiran. The loss of these warm, saline and somewhat more nutrient rich waters is compensated by the inflow of warm, nutrient depleted surface waters of the Red Sea (Plaehn et al., 2002). The winter mixing brings up nutrients from deep waters, which accumulate in the surface waters when spring stratification sets in. This generally leads to the initiation of a spring bloom in February–March. The microbial food web in both the northern Red Sea and Gulf of Aqaba are dominated by picoplankton (b2 μm) and ultraplankton (b 8 μm) mainly composed of cyanobacteria (Synechococcus sp.), Prochlorococcus sp. and diverse pico-eukaryotes (Stambler, 2005). In the Red Sea, throughout the year a deep chlorophyll maximum at about 50–60 m depth can be observed which is characterized by high concentrations of Prochlorococcus sp. that form about 50% of the total cell concentration, followed by Synechococcus sp. accounting for about 30% of the association. In the Gulf of Aqaba in summer a deep chlorophyll maximum can be observed at depths of about 80 m characterized by high concentrations of Prochlorococcus sp. whereas during the winter the phytoplankton association is well mixed though the water column consisting of eukaryotic phytoplankton (mainly diatoms), Prochlorococcus sp. (about 25% of the phytoplankton association) and Synechococcus sp. (about 50%). Dilution experiments reveal that of all phytoplankton groups, diatoms show the strongest response on increased nutrient availability as a result of mixing as well as nutrient limitation at the end of the mixing season whereas small organisms (pico- and

ultraplankton) showed little effects from nutrient limitation (Latasa et al., 1997; Post et al., 2002; Labiosa et al., 2003; Berninger and Wickham, 2005). Unfortunately there only very few plankton studies available that document the eukaryotic plankton composition in detail. Although no detailed studies are present from the northern Red Sea, plankton surveys from more southern parts of the Red Sea show that the eukaryotic species mainly consist of dinoflagellates and diatoms (Ostenfeld and Schmidt, 1902; Halim, 1969; Shaikh et al., 1986; Madkour et al., 2010; Nassar and Khairy, 2014; Nassar et al., 2014. Dinoflagellates have in general a higher species diversity but the large majority of eukaryoticc cells are formed by diatoms. The dinoflagellate association is mainly formed by species that can be assigned to the genera: Ceratium, Protoperidinium, Dinophysis and Gonyaulax. The toxic dinoflagellate species Pyrodinium bahamense which is frequently observed in the Red Sea, is considered to be one of the three main locations world-wide where this species is recorded (Usup et al., 2012). Due to the more pronounced seasonality variability of upper water hydrographic conditions in the Gulf of Aqaba, a larger seasonality in phytoplankton composition can be observed as well (Kimor and Golandsky, 1977; Al-Najjar et al., 2007). It is recorded that the main peak in eukaryotes, consisting of dinoflagellates, diatoms and tintinnids, occurs during the winter months. During this time, Prochlorococcus, that dominates the plankton during the stratified summer period, is almost absent. During winter relatively high proportions of Chlorophyceae and Cryptophyceae can be observed that are scarce or absent in summer. Diatoms and Synechococcus concentrations show sharp and moderate biomass peaks in late winter and spring respectively. Chrysophyceae, Prymnesiophyceae and Dinophyceae showed no clear seasonal distribution pattern.

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Fig. 2. Google Earth map (2014) of the northern part of the Gulf of Aqaba depicting sample positions and urbanized areas.

3. Material and methods 3.1. Sample collection and preparation 24 sediment samples were collected by multicoring during the RV Meteor expedition M44/3 in 1999 at water depths ranging from 240 to 1072 m (Pätzold et al., 1999; Figs. 1, 2). All recovered sediment samples consist of silty clay. Sediments of the Gulf of Aqaba are brownish in color, containing high amounts of terrigenous material and variable amounts of biogenic carbonate (Pätzold et al., 1999). Surface sediments (0–1 cm) were stored in a cool room (4 °C) immediately after recovery until palynological treatments. Palynological preparation has been executed using standardized laboratory procedures conform Elshanawany et al. (2010). A volume of 1–2 ml of wet sediment was treated with cold hydrochloric acid (HCl 10%) and cold hydrofluoric acid (HF 40%) to dissolve carbonate, and silicate minerals. The residual fraction of sediment was sonified and then sieved to eliminate particles smaller than 20 μm. The residue was centrifuged and transferred to Eppendorf tubes. A known volume of homogenized residual was mounted on microscopic slides with glycerin-gelatin jelly. The identification of dinocysts was carried out by light-microscopy at magnifications of 400× and 1000×. When slides contained less than 150 specimens, additional slides were counted (see Table 3). This number was determined on the basis of the estimation of the uncertainly in proportions and point counting based on the methods described by van der Plas and Tobi (1965) and Howarth (1998). Taxonomy follows the paleontological system of Fensome and Williams (2004) and Zonneveld and Pospelova (2015).

Dinoflagellate cysts were identified to species level except where orientation, folding and morphological similarities of specimens made this impossible. This was the case for most of the Spiniferites specimens. When specimens could not unequivocally be assigned to Spiniferites bentorii, Spiniferites membranaceus, Spiniferites mirabilis, or Spiniferites ramosus they were grouped in Spiniferites spp. No separation was made between S. bentorii and Spiniferites belerius. Specimens that could be assigned to this complex were grouped into S. bentorii. Echinidinium species were grouped into Echinidinium spp., because distinguishing morphological features could only be observed in rare cases. Relative abundances (%) of organic-walled dinoflagellate cysts have been calculated by dividing the cyst counts of individual species by the total cyst count. Absolute abundances (concentration) are calculated: Absolute abundances (concentration) (cyst g−1) = number of dinoflagellate cysts/g dried sediment. 3.2. Environmental parameters Annual and seasonal sea-surface temperature as well as chlorophylla (Chl a) data were obtained from Ocean Color Radiometry Online Visualization and Analysis (http://gdata1.sci.gsfc.nasa.gov/daac-bin/G3/gui. cgi?instance_id=ocean_month) based on 4 km resolution. Seasons are defined: winter: December–February, spring: March–May, summer: June–August, and autumn: September–November. Annual sea-surface salinity (anSSS), nitrate (anNit) and phosphate (anPho) concentration have been derived form the quarter-degree resolution data of the World Ocean Atlas 2013 of the National Oceanographic Data Center (http://www.nodc.noaa.gov/cgi-bin/OC5/SELECT/

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woaselect.pl). Unfortunately no information on these parameters was available in high enough resolution to allow the acquisition of seasonal data. 3.3. Statistical analyses Relationships between individual dinoflagellate cyst taxa and environmental parameters were investigated by the multivariate statistical methods Detrended Correspondence Analysis (DCA) and Redundancy Analysis (RDA). These analyses were performed using the software package CANOCO (version 4.02 for Windows). First a DCA was executed to test for linearity of the dataset (e.g., Ter Braak and Smilauer, 1998). The length of the first gradient in standard deviation units determines whether the assemblage shows unimodal variation (length N 2) or linear variation (length b 2) Since the length of the first gradient was lass than sd further analyses were performed using the linear based method of Redundancy Analysis. Two analyses have been executed: a. RDA1 which included the dinoflagellate cyst relative abundances and b. RDA2 including absolute abundance data (cyst g−1). Species occurring in one or two samples only, or occurring in percentages b0.5%, have been excluded from the analyses. The significance of each environmental variable was determined using a Monte Carlo permutation test, based on 500 permutations. Environmental variables with a P-value of less than 0.05 are considered to be significantly related to the cyst data. Covariance between parameters is determined by forward selection. Both the marginal effects (representing the amount of variance explained by the particular variable independent of potential covariability) and the conditional effects (representing the total amount of variance explained by the particular — variance related to covariabling parameters) were calculated for each variable. Groups of species were treated as separate entity as excluding them from the analysis would results in extremely reduced variability of the species data. The environmental parameters retained for statistical analyses include seasonal and annual temperature and chlorophyll-a concentrations, annual salinity, phosphate and nitrate concentration in surface waters as well as the water depth (Table 2). 4. Results 4.1. Dinoflagellate cyst assemblages A total of 35 taxa have been identified in the studied region (Table 1, Plates I–II). Cyst concentrations appear to be low to moderate with values ranging from ~400 to ~2250 cysts g−1 (Fig. 3). Cyst assemblages in the research area are dominated by Spiniferites spp. (about 56%) and to a lesser extent by Brigantedinium spp. (about 11%) and Operculodinium centrocarpum (9%). Relative to cysts produced by phototrophic species, cysts produced heterotrophic species form between 4.9% and 37.6% of the association. The heterotroph cyst association consist mainly of Brigantedinium spp. (~ 11%), Selenopemphix nephroides (4.5%), Votadinium calvum (~ 1%) and Echinidinium spp. (1%). The phototrophic cysts association mainly consists of Spiniferites spp. (~ 56%), O. centrocarpum (~ 9%), cysts of P. dalei (~ 5%), Operculodinium israelianum (~3%), S. mirabilis (~2.7%) and to a lesser extent Impagidinium aculeatum (2%), and Impagidinium sphaericum (2%). The species Polysphaeridium zoharyi, and Tuberculodinium vancampoae are observed in few stations and in low concentrations only (Fig. 3). Although there are some similarities, there are clear differences between the Red Sea and Gulf of Aqaba. Sediments of the Gulf of Aqaba are characterized by generally higher proportions of heterotrophic cysts compared to the Red Sea. The highest relative abundances of heterotrophic cysts can be found in the samples from locations just south of the cities of Eilat and Aqaba. The Heterotrophic cyst association in the Gulf of Aqaba consists mainly of Brigantedinium spp. and to a lesser extend of V. calvum, Echinidinium spp. and S. nephroides. V. calvum has the highest relative and absolute

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abundances in the Gulf of Aqaba compared to the Red Sea. Brigantedinium spp. has higher concentrations in the Gulf of Aqaba. Other heterotrophic species show comparable or lower abundances in the Gulf of Aqaba. Of the phototrophic species, Spiniferites spp., S. bentorii and S. mirabilis have higher relative abundances in the Gulf of Aqaba whereas I. aculeatum, I. sphaericum, cysts of P. dalei and O. israelianum have lower relative abundances in the Gulf. The distribution of L. machaerophorum is restricted to the Gulf of Aqaba where it occurs in low concentrations in few sites. These sites are located just south of the cities of Eilat and Aqaba (Figs. 2–3). In the Red Sea, autotrophic species largely dominate the assemblages. Their association consist mainly of Spiniferites spp., O. centrocarpum, O. israelianum and to a lesser extent of I. aculeatum, I. sphaericum and cysts of P. dalei. The distribution of Operculodinium longispinigerum is restricted to the Red Sea where it is observed in low concentrations only. The heterotrophic cyst association is mainly formed by S. nephroides and Brigantedinium spp. The lowest concentrations of heterotrophic cysts can be observed in the central Red Sea (Fig. 3). S. nephroides has higher cyst concentrations in the Red Sea compared to the Gulf of Aqaba (Fig. 3).

4.2. Statistical analyses 4.2.1. RDA1 Of the variables tested, only annual SSS, summer SST, annual chlorophyll-a, annual nitrate, annual SST and spring chlorophyll-a concentrations are significantly related (P b 0.05) to the cyst distribution. These environmental variables are well explaining the variation in the species data (37%, 32%, 27%, 26%, 25% and 24% respectively) (Table 3). Strong co-variance exists between annual phosphate and annual nitrate concentrations. After correction of this co-variance annual phosphate becomes insignificant (P value N0.05, explaining 2% of the variance in data set; Table 2). The variables annual nitrate and annual SSS point to the opposite direction as summer, annual SST, annual and spring chlorophyll-a. The species Brigantedinium spp., V. calvum, Echinidinium spp., L. machaerophorum, S. bentorii, S. membranaceus, Spiniferites spp., and S. mirabilis are ordinated at the positive side of the annual SSS and annual nitrate gradients and at the negative side of the temperature and chlorophyll-a gradients. The species I. aculeatum, I. sphaericum, O. israelianum, O. longispinigerum, O. centrocarpum, cysts of P. dalei, and S. nephroides are ordinated at the negative side of the nitrate and salinity gradient and at the positive side of the temperature and chlorophyll-a gradient (Fig. 4). Samples from the Gulf of Aqaba are ordinated at the positive site of these nitrate and salinity gradients, notably the samples that originate from locations just south of the cities of Eilat and Aqaba (Fig. 5).

4.2.2. RDA2 Results of the RDA2 analysis that are based on cyst concentrations, are only partly comparable to that of the RDA1 analysis that is based on the relative abundance data. Parameters spring SST and annual phosphate are significantly related to the variation in absolute cyst abundances (P b 0.05, Table 3). The species Echinidinium spp., Brigantedinium spp., V. calvum, S. mirabilis, S. bentorii, L. machaerophorum and to a lesser extent Spiniferites spp., are ordinated at the positive side of the annual nitrate, annual phosphate and annual SSS gradients and at the negative side of the temperature and chlorophyll-a gradients. The species I. aculeatum, I. sphaericum, O. israelianum, O. longispinigerum, cysts of P. dalei, and S. nephroides have moderate negative correlation with nitrate, phosphate and salinity gradients, while they have moderate positive correlation with temperature and chlorophyll-a gradients. The distribution of the other species, ordinated in the center of the gradients, is not related to one of the measured gradients (Fig. 6).

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R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44

Table 1 Species counts, and amount of gram counted. Station

5801–3

5802–2

5803–2

5804–2

5806–2

5808–3

5809–2

5810–3

5812–2

5813–1

5815–1

lat

29°24.90′

29°30.45′

29°30.96′

29°30.07′

29°22.75′

29°29.06′

29°30.40′

29°30.21′

29°31.14′

29°31.32′

29°30.64′

long

34°54.70′

34°57.68′

34°58.02′

34°57.44′

34°53.30′

34°56.35′

34°57.36′

34°57.73′

34°57.79′

34°57.90′

34°58.98′

depth

826 m

396 m

301 m

463 m

838 m

576 m

401 m

441 m

269 m

240 m

326 m

Ataxodinium choanum Bitectatodinium tepikiense Impagidinium aculeatum Impagidinium paradoxum Impagidinium patulum Impagidinium plicatum Impagidinium sphaericum Impagidinium spp. Lingulodinium machaerophorum Nematosphaeropsis labyrinthus Operculodinium centrocarpum Operculodinium israelianum Operculodinium janduchenei Operculodinium longispinigerum cyst of Pentapharsodinium dalei Polysphaeridium zoharyi Pyxidinopsis reticulata Spiniferites bentorii Spiniferites membranaceus Spiniferites mirabilis Spiniferites ramosus Spiniferites spp. Tuberculodinium vancampoae Brigantedinium spp. Echinidinium spp. Gymnodinium microreticulatum/nolleri Quinquecuspis concreta Selenopemphix nephroides Selenopemphix quanta Stelladinium stellatum Trinovantedinium applanatum Votadinium calvum Lejeunecysta sabrina Lejeunecysta oliva Xandarodinium xanthum Total counts Material processed (g) Material analyzed (g)

0 0 3 0 0 0 0 0 0 1 45 8 0 0 7 0 1 1 0 5 0 100 0 32 5 0 0 7 0 1 0 3 2 0 0 221 1.8703 0.37406

0 1 1 0 0 0 0 0 0 0 22 8 0 0 8 0 0 1 0 5 0 177 0 52 0 0 1 2 1 0 0 3 0 0 0 282 1.5878 0.31756

0 0 0 0 0 0 1 0 0 0 10 4 0 0 1 0 0 0 0 10 0 144 0 50 3 0 1 6 0 0 0 7 0 0 0 237 2.1064 0.42128

0 0 0 0 0 0 0 0 0 0 3 3 0 0 0 0 0 1 0 2 1 55 0 5 0 0 0 1 0 0 0 1 0 0 0 72 0.8921 0.17842

0 0 2 0 0 0 2 0 0 0 16 0 0 0 9 0 0 1 0 5 0 68 0 37 5 0 0 14 0 0 0 6 0 0 0 165 0.7357 0.07357

0 1 1 0 1 0 1 0 1 1 13 4 0 0 3 0 0 2 0 10 0 152 0 19 4 0 0 4 0 0 0 7 0 0 0 224 1.4217 0.28434

1 0 0 0 0 0 0 0 0 3 15 5 0 0 2 0 0 1 2 6 2 197 0 35 7 0 0 10 0 0 0 4 0 1 0 291 1.6145 0.16145

0 0 0 0 0 0 0 0 1 2 20 3 0 0 1 0 0 0 3 3 0 131 0 50 3 0 0 1 0 0 0 0 0 0 0 218 1.7045 0.17045

0 0 0 0 0 0 0 0 0 2 7 2 0 0 6 0 0 0 0 4 0 123 0 46 3 0 1 3 0 0 0 5 0 0 0 202 2.4735 0.24735

0 1 1 0 0 0 0 0 2 0 22 4 2 0 5 0 0 1 0 11 0 184 0 60 1 1 0 2 0 0 0 1 0 0 0 298 1.9943 0.19943

0 0 1 0 0 0 0 0 0 0 10 5 0 0 1 0 0 3 0 7 0 95 0 19 2 0 0 5 0 0 0 0 0 0 0 148 3.0115 0.30115

5. Discussion Our data show two dominant patterns. First, we observe a difference between dinoflagellate cyst association composition in the Gulf of Aqaba and the northern Red Sea. Second, we observe relatively moderate abundances of heterotrophic species up to (37.6%) in the Gulf of Aqaba and low relative abundances in the Red Sea.

5.1. Transport and preservation We assume that the differences in association between both basins are not caused by relocation of the species. Both basins are landlocked at three sides, and connected to adjacent seas by narrow sills reducing the exchange of water masses and suspended matter. The Red Sea is connected to the Arabian Sea by the narrow and shallow sill of 137 m minimum water depth at the Strait of Bab el Mandab in the far south (Smeed, 2004). The Gulf of Aqaba is connected to the Red Sea by the Strait of Tiran (242 m), with a near-surface water inflow into the Gulf and an underlying outflow. Since the sill in the Strait of Tiran is relatively shallow, we assume minimal sediment transport between the basins over the sill. In both basins ocean bottom waters are well-ventilated and high bottom water oxygen concentrations exist. This could have resulted in selective degradation of cyst species vulnerable to aerobic degradation,

notably those produced by heterotrophic species (e.g. Brigantedinium spp., Echinidinium spp., V. calvum, S. nephroides, Zonneveld et al., 2008). Consequently, the absolute abundance data of the heterotrophic cyst species can be considered to represent minimal concentrations and it can be assumed that actual accumulation rates might have been higher. However, cysts resistant against aerobic degradation, notably Impagidinium species, O. israelianum, Nematosphaeropsis labyrinthus, and cysts of P. dalei are minimally altered and it can be assumed that their absolute abundances reflect their initial production. Their relative abundances might however, be overrepresented relative to the sensitive species. We assume that associations in both basins might have undergone an equivalent rate of aerobic overprint. This implies that although the relative and absolute abundances of heterotrophic cysts could represent underestimated values, it can be expected that the spatial differences between heterotrophic species still reflects differences in their initial production.

5.2. Cyst distribution in comparison to environmental conditions The sedimentary dinocyst concentrations in the research area range from ~ 400 to ~ 2250 cysts/g). These concentrations are in range or somewhat higher than cyst concentration observed in the most oligotrophic regions in the world where sediments have been studied for

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35

5823–1

5824–1

5825–1

5828–1

5831–1

5832–1

5837–1

5838–1

5839–2

5840–1

5842–1

5843–2

5844–1

26°25.26′

26°29.12′

26°30.47′

26°20.78′

27°05.30′

27°03.20′

27°36.69′

27°34.54′

27°34.84′

27°31.66′

27°42.70′

27°52.69′

27°42.81′

35°40.19′

35°49.52′

35°56.94′

35°24.13′

35°33.98′

35°24.32′

34°51.85′

34°44.16′

34°47.92′

34°41.24′

35°02.84′

34°58.16′

34°40.94′

789 m

587 m

1031 m

1072 m

884 m

628 m

771 m

832 m

803 m

908 m

863 m

529 m

963 m

0 0 11 2 1 0 5 5 0 2 15 11 0 4 6 0 0 0 0 1 1 71 0 4 0 0 0 3 0 0 1 0 0 0 0 143 1.8709 0.18709

0 0 8 2 0 0 8 2 0 0 25 5 0 0 9 1 0 0 0 3 0 69 0 19 2 0 0 14 0 0 1 0 0 0 1 169 2.3029 0.92116

0 0 4 0 0 0 3 0 0 0 19 3 1 1 24 0 0 0 0 1 0 78 0 10 1 0 0 12 0 0 0 0 0 0 0 157 1.5995 0.15995

0 0 9 0 0 0 5 0 0 0 32 16 0 0 25 0 1 1 0 6 0 88 0 3 3 0 0 5 0 0 0 0 0 0 0 194 1.9044 0.76176

0 0 7 0 0 1 15 0 0 1 19 10 0 5 30 0 0 0 0 3 0 96 0 15 1 0 0 17 0 0 0 0 1 0 0 221 0.7448 0.07448

0 1 5 0 0 0 6 0 0 0 19 8 0 1 9 0 0 0 0 1 4 87 0 5 3 0 0 29 0 0 0 1 0 0 0 179 2.0412 0.20412

0 0 5 0 0 0 4 0 0 0 12 9 0 0 5 0 0 0 0 4 0 79 0 9 0 0 0 15 1 0 1 0 0 0 0 144 2.0035 0.20035

0 0 5 0 0 1 5 0 0 0 15 6 0 0 7 0 0 0 0 4 0 98 0 3 1 0 0 4 0 0 1 0 0 0 0 150 2.623 0.2623

0 0 6 0 0 0 14 0 0 0 8 4 0 0 8 0 0 0 0 10 0 116 1 8 0 0 0 6 0 0 4 0 0 0 0 185 2.5603 0.25603

0 0 12 0 0 0 9 0 0 0 17 13 0 0 5 0 0 2 0 16 1 90 1 1 1 0 1 5 0 0 0 0 0 1 0 175 2.3838 0.95352

0 0 7 0 0 0 6 0 0 3 20 10 0 3 23 0 0 1 0 5 2 111 1 9 1 0 0 27 0 0 0 0 0 0 0 229 1.6695 0.16695

0 0 3 0 1 0 5 0 0 1 11 7 0 4 20 0 0 0 1 1 1 90 0 8 0 0 0 7 0 0 2 0 0 0 0 162 0.8853 0.17706

0 0 6 0 2 0 6 0 0 0 5 8 0 0 11 2 0 0 0 0 0 104 0 8 2 0 0 11 0 0 0 4 0 0 0 162 1.2639 0.50556

dinoflagellate cyst concentrations so far. In these regions, such as the central South Atlantic Ocean, the central north Pacific Ocean and the central Eastern Mediterranean Sea, cyst concentrations generally range from 0 to about 1000 cysts/g (e.g. Vink et al., 2000; Esper and Zonneveld, 2002; Holzwarth et al., 2007, 2010; Pospelova et al., 2008; Elshanawany et al., 2010; Krepakevich and Pospelova, 2010; Limoges et al., 2013). Concentrations are, as expected, much lower compared to eutrophic regions such as upwelling regions, river plume systems, eutrophic coastal areas etc. For instance in upwelling regions of the southeastern Atlantic, off NW Africa and northeastern Pacific Ocean, cyst concentrations can be as high as 38,580 cysts/g, 3500 cysts/g and 35,000 cysts/g respectively (Holzwarth et al., 2007; Pospelova et al., 2008; Bouimetarhan et al., 2008; Holzwarth, 2009, 2010). Krepakevich and Pospelova (2010) reported dinocyst concentrations of about 25,000 cysts/g in Canadian coastal bays. We observed 35 cyst species in the studied sediments. Tese are more species as previously have been recorded in plankton surveys of the Gulf of Aqaba and the Red Sea. Plankton surveys only 6 phototrophic species (Gonyaulax scripssiae ∼ S. belerius, Gonyaulax spinifera ∼ N. labyrinthus, S. mirabilis, S. ramosus, Protoceratium reticulata ∼ O. centrocarpum and Pyrophacus steinii ∼ T. vancampoae) and 5 heterotrophic species (Diplopsalis lenticulata ∼ Brigantedinium spp., Protoperidinium compressum ∼ S. stellatum, Protoperidinium conicum ∼ Selenopemphix quanta, Protoperidinium leonis ∼ Quinquesuspis concreta and Protoperidinium oblongum ∼ V. calvum) (Ostenfeld and Schmidt, 1902; Madkour et al.,

2010; Nassar and Khairy, 2014). The high number in our study is logical as plankton surveys that are available for the region do not provide information about long-term continuous surveys but from momentum recordings only. The upper sediments studied here have been accumulated over several years and as such, represent cyst production over the complete time interval of deposition. Based on the sediment accumulation estimations of gravity cores from the Gulf of Aqaba, sediments of this region represent deposition of about 20–30 years (Lamy et al., 2006). Unfortunately no detailed information about the sedimentation rates in the northern Red Sea are available but we assume that upper sediments represent comparable periods of time. Based on visual examination of the data and the multivariate ordination techniques we can clearly distinguish two associations characteristic for the Gulf of Aqaba and the Red Sea respectively. The cyst species that have their highest concentrations in the Gulf of Aqaba are ordinated at the positive side of the annual SSS and annual nitrate (and covarying phosphate) concentration gradients and at the negative side of the annual temperature and spring chlorophyll-a gradients. Due to higher evaporation rates in the Gulf, surface salinity concentrations are higher in the Gulf compared to the northern Red Sea. Stronger seasonal contrasts with more severe cooling in winter results in somewhat lower annual temperature values in the Gulf. In the Gulf of Aqaba nutrient concentrations are higher in winter and early spring due to winter mixing resulting in somewhat higher annual concentrations of nitrate and phosphate (e.g. Berninger and Wickham, 2005; Stambler, 2005).

36

R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44

Table 2 Sample coordinates (latitude °N, longitude °E) and environmental variables used for the multivariate analysis. The missing numbers are not available. Station

5801–3 5802–2 5803–2 5804–2 5806–2 5808–3 5809–2 5810–3 5812–2 5813–1 5815–1 5823–1 5824–1 5825–1 5828–1 5831–1 5832–1 5837–1 5838–1 5839–2 5840–1 5842–1 5843–2 5844–1

Lat (°N)

29°24.90′ 29°30.45′ 29°30.96′ 29°30.07′ 29°22.75′ 29°29.06′ 29°30.40′ 29°30.21′ 29°31.14′ 29°31.32′ 29°30.64′ 26°25.26′ 26°29.12′ 26°30.47′ 26°20.78′ 27°05.30′ 27°03.20′ 27°36.69′ 27°34.54′ 27°34.84′ 27°31.66′ 27°42.70′ 27°52.69′ 27°42.81′

Long (°E)

34°54.70′ 34°57.68′ 34°58.02′ 34°57.44′ 34°53.30′ 34°56.35′ 34°57.36′ 34°57.73′ 34°57.79′ 34°57.90′ 34°58.98′ 35°40.19′ 35°49.52′ 35°56.94′ 35°24.13′ 35°33.98′ 35°24.32′ 34°51.85′ 34°44.16′ 34°47.92′ 34°41.24′ 35°02.84′ 34°58.16′ 34°40.94′

Depth

826 m 396 m 301 m 463 m 838 m 576 m 401 m 441 m 269 m 240 m 326 m 789 m 587 m 1031 m 1072 m 884 m 628 m 771 m 832 m 803 m 908 m 863 m 529 m 963 m

Annual

Winter

Spring

Summer

Autumn

Annual

Winter

Spring

Summer

Autumn

Annual

Annual

Annual

SST (°C)

SST (°C)

SST (°C)

SST (°C)

SST (°C)

Chla

Chla

Chla

Chla

Chla

SSS

N

P

23.73 24.25 24.25 24.58 23.97 23.97 24.21 24.59 24.25 24.25 24.25 24.25 26.02 26.15 26.28 25.74 25.98 25.92 25.26 25.45 25.05 25.61 25.57 25.25

21.14 21.09 21.09 21.43 20.94 21.14 21.49 21.09 21.09 21.09 21.09 22.27 22.16 22.32 22.22 22.04 22.04 21.86 21.54 21.64 21.71 21.84 21.79 21.73

22.92 23.71 23.71 23.97 23.23 23.68 23.96 23.71 23.71 23.71 23.71 25.15 25.20 25.44 24.91 24.98 24.72 24.34 24.11 24.23 24.10 24.67 24.81 24.17

27.17 26.77 26.77 26.82 26.29 26.72 26.82 26.77 26.77 26.77 26.77 28.48 28.75 28.88 28.36 28.57 28.16 27.69 27.24 27.54 27.21 28.06 28.02 27.31

23.60 23.89 23.89 23.93 23.90 23.96 23.93 23.89 23.89 23.89 23.89 26.42 26.46 26.47 26.07 26.37 26.23 25.64 25.41 25.67 25.41 25.84 25.67 25.73

0.16

0.19

0.12

0.07

0.18

0.21 0.13

0.19 0.21

0.12 0.08

0.07 0.06

0.16 0.21

0.11 0.11 0.12 0.13 0.12 0.12 0.13 0.14 0.14 0.14 0.14 0.15 0.14

0.22 0.22 0.21 0.23 0.22 0.24 0.34 0.23 0.34 0.29 0.28 0.27 0.32

0.11 0.10 0.09 0.13 0.10 0.11 0.14 0.18 0.15 0.19 0.14 0.14 0.15

0.05 0.05 0.06 0.06 0.06 0.06 0.07 0.07 0.07 0.07 0.08 0.10 0.08

0.10 0.10 0.11 0.09 0.12 0.11 0.11 0.11 0.11 0.10 0.13 0.15 0.12

40.64 40.79 40.79 40.79 40.64 40.64 40.79 40.79 40.79 40.79 40.79 40.11 40.06 40.14 40.19 40.20 40.22 40.34 40.36 40.34 40.36 40.30 40.36 40.36

2.14 2.14 2.14 2.14 2.14 2.14 2.14 2.14 2.14 2.14 2.14 0.45 0.45 0.45 0.45 0.30 0.30 0.10 0.10 0.10 0.10 0.20 0.10 0.10

0.27 0.27 0.27 0.27 0.27 0.27 0.27 0.27 0.27 0.27 0.27 0.16 0.16 0.16 0.16 0.03 0.03 0.09 0.09 0.09 0.09 0.30 0.09 0.09

Due to permanent nutrient limitation in both basins, chlorophyll-a concentrations are very low. In both basins, a deep chlorophyll maximum is present. In the Gulf chlorophyll-a is distributed more equally through the water column in winter due to mixing. Chlorophyll-a concentrations at the surface are slightly higher in the Red Sea compared to the Gulf, notably during the spring bloom, concentrations at the chlorophyll maximum are however lower. We therefore assume that although statistically chlorophyll-a is a significant factor, it is not a causal factor influencing cyst production. It is most likely that cyst production does not take place at the surface of the water column but in the deep chlorophyll maximum. In the north of the Gulf of Aqaba local enhanced nutrient input can be found as a result of anthropogenic activities around the cities of Eilat and Aqaba (e.g. Berninger and Wickham, 2005). We observe that two species have distributions either restricted to the Gulf of Aqaba (L. machaerophorum), or with the highest abundance at these locations (V. calvum). During the last decades, phytoplankton studies reveal that the plankton associations have changed related to eutrophication from anthropogenic sources, such as sewage and fish farms, that are located in the northern part of the Gulf of Aqaba (e.g., Laiolo et al., 2014). Previous studies on the cyst production and geographic distribution of dinoflagellate cysts in other regions of the world show that both L. machaerophorum and V. calvum show a positive correlation with anthropogenic eutrophication (especially with nitrate e.g. Dale, 2009; Satta et al., 2010; Shin et al., 2010a, 2010b; Zonneveld et al., 2012, 2013). We therefore suggest that the occurrence of L. machaerophorum and higher abundances of V. calvum may be related to the anthropogenic activities in the Gulf of Aqaba. Apart from the above-mentioned species, the species Brigantedinium spp., Echinidinium spp., Spiniferites spp., S. bentorii, S. membranaceus and S. mirabilis have higher relative and absolute abundances in the Gulf compared to the Red Sea. Our results suggest that these species benefit more than the other species from the somewhat higher nutrient concentrations in the Gulf in comparison. For the phototrophic species, this relationship could be a direct causal relationship with the somewhat enhanced nutrient concentrations resulting in higher growth

rates. However, both the above mentioned phototrophic species as the heterotrophic species are known to be able to ingest other organisms and as such their enhanced cyst concentrations in the Gulf might be related to the higher abundance of prey as well (see next chapter). We observe a strong positive relationship between the relative abundances of I. aculeatum, I. sphaericum, O. israelianum, O. longispinigerum and cysts of P. dalei with the temperature and chlorophyll-a gradients. A negative relationship is observed with the nitrate, phosphate and salinity gradients. This negative relationship indicates that these species might be better adapted to the extreme oligotrophic conditions in the northern Red Sea compared to the Gulf of Aqaba. This supports literature based observations that I. aculeatum and I. sphaericum are often observed in high relative abundances in oligotrophic environments (e.g. Zonneveld et al., 2013; Limoges et al., 2013). However, studies on sediment traps and cyst accumulation rates document that their cyst production is often enhanced when more micro- and macronutrients become available in the upper water column (e.g. Zonneveld and Brummer, 2000; Zonneveld et al., 2010). This suggests that although these species can tolerate the oligotrophic to extreme oligotrophic conditions in the upper water column they are not restricted to these environments. In the current study O. israelianum dominates the warmer, deeper, and lower salinity sampling sites in the northern Red Sea. The positive relation between the relative abundance of this species with temperature is in accordance with previous studies (e.g. Marret and Zonneveld, 2003; Pospelova et al., 2004; Zonneveld et al., 2009; Elshanawany et al., 2010), which reveal that O. israelianum is restricted to fullmarine regions and can dominate assemblages in high salinity environments such as shallow lagoons in sub-tropical–tropical regions (Bradford and Wall, 1984; Morzadec-Kerfourn et al., 1990; Zonneveld et al., 2013). This is in not in contrast with our finding, since although the dinoflagellate cyst distribution is significantly related to the salinity gradient in the region, the complete gradient lies in the upper part of the “world-wide” salinity levels with high salinities at all sampling points (N 40 psu).

Plate I. Micrographs of selected dinocyst taxa from the study area. Scale bars are 10 μm. 1. Nemaosphaeropsis labyrinthus. 2–3. Impagidinium aculeatum. 4. Impagidinium paradoxum. 5–6. Impagidinium sphaericum. 7–8. Polysphaeridium zoharyi. 9. Operculodinium longispinigerum. 10. Operculodinium israelianum. 11. Operculodinium centrocarpum. 12–13. Echinidinium spp. 14– 15. Brigantedinium spp.

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Plate II. Micrographs of selected dinocyst taxa from the study area. Scale bars are 10 μm. 1–2. Cysts of Pentapharsodinium dalei. 3. Trinovantedinium applanatum. 4. Spiniferites mirabilis. 5–10. Spiniferites spp. 11. Lingulodinium machaerophorum. 12. Selenopemphix nephroides.

We observe O. longispinigerum in a few sites from the northern Red Sea. Results from RDA1 and RDA2 document that the relative and absolute abundance of this species is positively correlated with temperature, while a negative correlation with annual nitrate and phosphate concentration exists. This is in agreement with previous studies. Zonneveld et al. (2013) reported that this species is commonly observed in tropical oligotrophic environments from the south of the Indonesian island Java

and concluded that this species occurs in tropical to equatorial, fullmarine, oligotrophic environments. We observe relatively high abundances of cysts of P. dalei. This species is generally observed in cold, stratified nutrient rich waters often related to regions that are influenced by ice melting waters (e.g. Solignac et al., 2009; Pospelova et al., 2010; Price and Pospelova, 2011; Heikkilä et al., 2014). Apart from stratification, these regions have no

R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44

39

Fig. 3. Relative abundance data (%) and absolute abundance data (cyst/g dry sediment) of dinoflagellate cyst species in surface sediments from the northern Red Sea and Gulf of Aqaba. Taxa below dashed line are autotrophic taxa, while taxa above it are heterotrophic.

environmental characteristics in common with the investigated tropical ecosystems. However, the global distribution of this species shows distinct clusters of distribution along the global temperature, salinity and environmental parameter gradients (Zonneveld et al., 2013). Zonneveld et al. (2013) document a multimodal pattern (several optima) of the distribution curves of cysts of P. dalei in relation to environmental gradients. Such a relationship can typically occur when more than one species have been included into one morphologic entity. This can be the result either of incorrect identification of the species or of the presence of cryptic species. Our findings imply that more research

about the genetic character of this species is needed to shed light on this phenomenon. Surprisingly we observe very low abundances of P. zoharyi in the study area. This is remarkable as this species is extremely abundant in downcore sediments from the central Red Sea where changes in relative abundance have been used to reconstruct sea level changes (Wall and Warren, 1969). This species can be dominantly present in shallow water lagoons that are characterized by high salinity concentrations (Zonneveld et al., 2013 and references therein). To date such lagoons are not present in the vicinity of our sampling sites, which may explain

40

R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44

Table 3 Analysis of the significance of environmental variables in the Redundancy Analysis (RDA) of relative abundance and absolute abundance data respectively. Statistical significance (P b 0.05) variables based on Monte Carlo permutations with 500 iterations in forward selection. Variance explained is given based on forward selection and when the variable is used as sole variable exclusively. Variable

Explained as sole variable (%)

P-value

Explained after forward selection (%)

RDA-1 Annual SST Winter SST Spring SST Summer SST Autumn SST Annual chlorophyll-a Winter chlorophyll-a Spring chlorophyll-a Summer chlorophyll-a Autumn chlorophyll-a Annual SSS Annual nitrate Annual phosphate Water depth

25 28 20 32 31 27 24 24 25 18 37 26 24 27

0.05 0.07 0.43 0.05 0.70 0.03 0.08 0.01 0.36 0.23 0.00 0.02 0.13 0.30

5 7 1 3 0 7 6 8 2 1 37 10 2 1

RDA-2 Annual SST Winter SST Spring SST Summer SST Autumn SST Annual chlorophyll-a Winter chlorophyll-a Spring chlorophyll-a Summer chlorophyll-a Autumn chlorophyll-a Annual SSS Annual nitrate Annual phosphate Water depth

1 1 2 15 1 14 1 11 3 3 6 0 12 2

0.62 0.52 0.41 0.01 0.52 0.06 0.47 0.11 0.27 0.26 0.10 0.94 0.05 0.48

7 8 5 7 9 4 11 11 7 3 4 11 6 11

the low abundance in our dataset. This might have been different in the past at times when sea level was lower. We suggest that this might be a possible cause for the relative high downcore abundance of this species.

Fig. 5. Ordination diagram of the RDA1 sample scores (relative abundance data). Open circles represent samples from the Gulf of Aqaba, closed circles represent Red Sea samples.

5.3. Cyst distribution versus food web We observe in the nutrient depleted ecosystems of the northern Red Sea and Gulf of Aqaba cysts of both phototrophic and heterotrophic species. Many, if not all of the phototrophic dinoflagellates are known to be mixotrophic and are able to ingest other organisms (e.g. Bockstahler and Coats, 1993; Taylor et al., 2008). Consequently, their distribution might be related to that of their prey, similar as can be expected for heterotrophic dinoflagellates. Until now this aspect has not been studied.

Fig. 4. Ordination diagram of the RDA1 species scores (relative abundance data) and environmental variables.

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41

Fig. 6. Ordination diagram of the RDA2 species scores (absolute abundance data) and environmental variables.

In our research area, we observe higher concentrations of cysts of L. machaerophorum, S. bentorii, S. membranaceus, S. mirabilis and Spiniferites spp. in the Gulf of Aqaba compared to the Red Sea. The phytoplankton association in both the northern Red Sea and the Gulf of Aqaba is dominated by picoplankton (b 2 μm) and ultra-plankton (b8 μm) (Lindell and Post, 1995; Yahel et al., 1998), in line with the general observations in extremely oligotrophic lakes and seas (Stockner and Antia, 1986; Li et al., 1993). The success of the smallest phytoplankton size classes is frequently ascribed to their enhanced ability for retrieving mineral nutrients in a very diluted environment because of their favorable surface:volume ratio (Raven, 1986). The phytoplankton assemblages in the Gulf of Aqaba and the northern Red Sea are however significantly different. Although in both regions they are composed of three groups of organisms; cyanobacteria (mainly Synechococcus spp.), Prochlorococcus spp., and diverse pico-eukaryotes the deep chlorophyll maximum in the Red Sea is inhabited by high concentrations of Prochlorococcus (~ 75%), whereas in the Gulf of Aqaba, the eukaryotic algae (~20%), Synechococcus spp. (~50%), and Prochlorococcus (~25%), are observed (Stambler, 2005). Jeong et al. (2005) documented that the motile forms of L. machaerophorum and the Spiniferites species

(Lingulodinium polyedrum and G. spinifera) are able to ingest Synechococcus whereas they could not determine a predator–prey relationship between dinoflagellates and Prochlorococcus spp. Integrating this information with our observations leads to the suggestion that the higher abundances of Lingulodinium and Spiniferites species in the Gulf of Aqaba might be related to the higher abundances of Synechococcus in the Gulf compared to the Red Sea. This aspect deserves more attention in the future as it might be a previous overlooked important factor influencing phototrophic dinoflagellate cyst distribution. We therefore suggest future cyst distribution studies to combine digital data of prey organism distribution with dinocyst data in the statistical analysis in order to test this interpretation. The distribution of heterotrophic dinoflagellates cysts can often be linked to the distribution of the prey of their motile forms (e.g. Zonneveld et al., 2010; Heikkilä et al., 2014 and references therein). Here we observe relatively high concentrations of the heterotrophic species Brigantedinium spp., Echinidinium spp. and V. calvum in the Gulf of Aqaba whereas high relative abundances of S. nephroides can be observed in the northern Red Sea. Numerous studies document that diatoms can form the prey of several species of Protoperidinium

42

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that produce cysts of Brigantedinium spp. and Echinidinium spp. (e.g. Jacobson and Anderson, 1986; Jeong et al., 2010). Several studies correlated the production of diatoms with the production and distribution of Brigantedinium spp. (Fujii and Matsuoka, 2006; Pospelova et al., 2010 and Price and Pospelova, 2011). The sediment trap records from the Saanich Inlet (BC. Canada) and off NW Africa reveal that the production of V. calvum (cyst of Protoperidinium latidorsale) has a positive correlation with the production of opal (reflecting diatom production) and total organic matter in the upper waters. Compared to the northern Red Sea, the Gulf of Aqaba hosts higher concentrations of eukaryotic phytoplankton (diatoms). Labiosa et al. (2003) showed that the phytoplankton community structure exhibits strong seasonality in the Gulf of Aqaba, with Synechococcus and Prochlorococcus dominating during the spring and summer, respectively, and eukaryotic phytoplankton (notably diatoms) dominating during winter. According to the phytoplankton studies in the Gulf, diatoms responded most strongly to increased nutrients during mixing, gradually decreased during the summer, when nutrients become more limited (Latasa et al., 1997; Post et al., 2002). Berninger and Wickham (2005) demonstrated that in the Gulf of Aqaba and northern Red Sea the small organisms (pico-, and ultra-plankton) showed little nutrient limitation but susceptibility to grazing, whereas the larger microalgae (especially diatoms) were relatively more affected by nutrient limitation. This suggests that the higher abundances of V. calvum, Brigantedinium spp. and Echinidinium spp. might be related to the abundance of diatoms. We observe higher relative abundances of S. nephroides (cyst of Protoperidinium subinerme, according to Wall and Dale, 1968) in the northern Red Sea. Until now, no details are available about the predator–prey relationship of Protoperidnium subinerme. However, sediment trap studies fail to determine a relationship between cyst production of this species with opal or biogenic silica concentrations (e.g. Pospelova et al., 2010; Zonneveld et al., 2010; Bringué et al., 2013). Zonneveld et al. (2013) observed a positive relationship between the cyst production of this species and total organic matter. Visual examination of the trap data of Pospelova et al. (2010) shows a similar pattern. We therefore assume that the prey of this species is different to that of Brigantedinium spp., Echinidinium spp. and V. calvum. Of course, these suggestions are very speculative and predator–prey experiments are needed to confirm or reject our hypothesis. 6. Conclusions Although sediments of the extreme oligotrophic ecosystems of the northern Red Sea and Gulf of Aqaba contain cysts of both phototrophic and heterotrophic dinoflagellates, cysts of phototrophic species dominate both basins. A clear difference between the dinoflagellate cyst associations of the two basins has been observed. L. machaerophorum is characteristically observed in the Gulf of Aqaba. In this basin, V. calvum, Brigantidinium spp., Echinidinium spp., Spiniferites species have higher abundances. The species I. aculeatum, I. sphaericum, O. israelianum, O. longispinigerum, O. centrocarpum, cysts of P. dalei and S. nephroides have higher relative abundances in the northern Red Sea. Both V. calvum and L. machaerophorum have higher densities in the samples south of the cities of Aqaba and Eilat at sites where upper waters are influenced by anthropogenic pollution. The distribution of both heterotrophic and phototrophic species shows a strong relationship with the composition of the phytoplankton community in both basins, that is composed of cyanobacteria (mainly Synechococcus spp.), Prochlorococcus spp., and diverse pico-eukaryotes. The deep chlorophyll maximum in the Red Sea is inhabited by high concentrations of Prochlorococcus (~75%), whereas in the Gulf of Aqaba, eukaryotic algae (~20%), Synechococcus spp. (~50%), and Prochlorococcus (~ 25%), are typical. Cysts of heterotrophic dinoflagellates that are known to feed on diatoms (Brigantedinium spp., Echinidinium spp. and V. calvum) have their highest abundance in the Gulf of Aqaba suggesting

a strong relationship between the distribution of predator and prey. S. nephroides is more abundant in the Red Sea suggesting that this species prefers other food sources as eukaryotes. Cysts of phototrophic dinoflagellate species that are known to be able to ingest Synechococcus spp. (L. machaerophorum and Spiniferites species) are most abundant in the Gulf of Aqaba suggesting that a predator–prey relationship might influence the cyst distribution of mixotrophic dinoflagellates as well. In the future, more detailed surveys on predator prey relationships and their distribution in water column and sediment are needed to confirm the here suggested relationships between cysts of both mixotrophic and heterotrophic dinoflagellates and their potential prey. Acknowledgements This research is funded by the German Science Foundation (DFG) funded centre of excellence MARUM and the Egyptian Cultural Affairs and Missions Sector in form of a scholarship of Dr. R. Elshanawany. References Afargan, H., Gildor, H., 2015. The role of the wind in the formation of coherent eddies in the Gulf of Eilat/Aqaba. J. Mar. Syst. 142, 75–95. Al-Najjar, D., Badran, M.I., Richter, C., Meyerhoefer, M., Sommer, U., 2007. Seasonal dynamics of phytoplankton in the Gulf of Aqaba, Red Sea. Hydrobiologia 579, 69–83. Badran, M.I., 2001. Dissolved oxygen, chlorophyll a and nutrients: seasonal cycles in waters of the Gulf of Aquaba, Red Sea. Aquat. Ecosyst. Health Manag. 4, 139–150. Berninger, U.-G., Wickham, S.A., 2005. Response of the microbial food web to manipulation of nutrients and grazers in the oligotrophic Gulf of Aqaba and the nothern Red Sea. Mar. Biol. 147, 1017–1032. Bockstahler, K.R., Coats, D.W., 1993. Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J. Eukaryot. microbiol. 40, 49–60. Bouimetarhan, I., Marret, F., Dupont, L., Zonneveld, K., 2008. Dinoflagellate cyst distribution in marine surface sediments off West Africa (17-6°N) in relation to seasurface conditions, freshwater input and seasonal coastal upwelling. Mar. Micropaleontol. 71, 113–130. Bradford, M.R., Wall, D.A., 1984. The distribution of recent organic-walled dinoflagellate cysts in the Persian Gulf, Gulf of Oman, and northwestern Arabian Sea. Palaeontogr. Abt. B 192, 16–84. Bravo, I., Figueroa, R.I., 2014. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2, 11–32. Bringué, M., Pospelova, V., Pak, D., 2013. Seasonal production of organic-walled dinoflagellate cysts in an upwelling system: a sediment trap study from the Santa Barbara Basin, California. Mar. Micropaleontol. 100, 34–51. Dale, B., 1996. Dinoflagellate cyst ecology: modeling and geological applications. In: Jansonius, J., McGregor, D.C. (Eds.), Palynology: Principles and Applications 3. American Association of Stratigragphic Palynologists. Foundation, College Station TX, pp. 1249–1275. Dale, B., 2009. Eutrophication signals in the sedimentary record of dinoflagellate cysts in coastal waters. J. Sea Res. 61, 103–113. Dale, B., Fjellså, A., 1994. Dinoflagellate cysts as productivity indicators: state of the art, potential and limits. In: Zahn, R. (Ed.), Carbon Cycling in the Glacial Ocean: Constraints in the Ocean's Role in Global Change. Springer, Berlin, pp. 521–537. de Vernal, A., Henry, M., Matthiessen, J., Mudie, P.J., Rochon, A., Boessenkool, K.P., Eynaud, F., Grosfjeld, K., Guiot, J., Hamel, D., Harland, R., Head, M.J., Kunz-Pirrung, M., Levac, E., Loucheur, V., Peyron, O., Pospelova, V., Radi, T., Turon, J.L., Voronina, E., 2001. Dinoflagellate cyst assemblages as tracers of sea-surface conditions in the northern North Atlantic, Arctic and sub-Arctic seas: the new ‘n-677’ data base and its application for quantitative palaeoceanographic reconstruction. J. Quat. Sci. 16, 681–698. de Vernal, A., Eynaud, F., Henry, M., Hillaire-Marcel, C., Londeix, L., Mangin, S., Matthiessen, J., Marret, F., Radi, T., Rochon, A., Solignac, S., Turon, J.L., 2005. Reconstruction of sea surface conditions at middle to high latitudes of the northern hemisphere during the last glacial maximum (LGM) based on dinoflagellate cyst assemblages. Quat. Sci. Rev. 24, 897–924. Elshanawany, R., Zonneveld, K.A.F., Ibrahim, M.I., Kholeif, S.E.A., 2010. Distribution patterns of recent organic-walled dinoflagellate cysts in relation to environmental parameters in the Mediterranean Sea. Palynology 34, 233–260. Esper, O., Zonneveld, K.A.F., 2002. Distribution of organic-walled dinoflagellate cysts in surface sediments go the Southern Ocean (Atlantic Sector) between the subtropical front and Weddell Gyre. Mar. Micropaleontol. 46, 177–208. Fensome, R.A., Williams, G.L., 2004. The Lentin and Williams Index of fossil dinoflagellates. American Association of Stratigraphic Palynologists Foundation Contribution Series 42 (909 pp.). Fujii, R., Matsuoka, K., 2006. Seasonal change of dinoflagellates cyst flux collected in a sediment trap in Omura Bay, West Japan. J. Plankton Res. 28, 131–147. Genin, A., Lazar, B., Brenner, S., 1995. Vertical mixing and coral death in the Red Sea following the eruption of Mount Pinatubo. Nature 112, 507–510. Gómez, F., 2005. A list of free-living dinoflagellate species in the world's oceans. Acta Bot. Croat. 64 (1), 129–212. Halim, Y., 1969. Plankton of the Red Sea. Oceanogr. Mar. Biol. Annu. Rev. 7, 231–275.

R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44 Heikkilä, M., Pospelova, V., Hochheim, K.P., Zou, Z., Kuzyk, A., Stern, G.A., Barber, D.G., Macdonald, R.W., 2014. Surface sediment dinoflagellate cysts from the Hudson Bay system and their relation to freshwater and nutrient cycling. Mar. Micropaleontol. 106, 79–109. Holzwarth, U., Esper, O., Zonneveld, K., 2007. Distribution of organic-walled dinoflagellate cysts in shelf surface sediments of the Benguela upwelling system in relationship to environmental conditions. Mar. Micropaleontol. 64, 91–119. Holzwarth, U., Esper, O., Zonneveld, K.A.F., 2010. Organic-walled dinoflagellate cysts as indicators of oceanographic conditions and terrigenous input in the NW African upwelling region. Rev. Palaeobot. Palynol. 159, 35–55. Holzwarth, U., 2009. Characterization of West African upwelling areas based on organicwalled dinoflagellate cysts and their application in the fossil record (PhD Thesis) Bremen University, p. 229. Hoppenrath, M., Elbrächter, M., Drebes, G., 2009. Marine phytoplankton. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, pp. 1–264. Howarth, R.J., 1998. Improved estimations of uncertainty in proportions, point-counting, and pass-fail test results. Am. J. Sci. 298, 594–607. Houben, A.J., Bijl, P.K., Pross, J., Bohaty, S.M., Passchier, S., Stickley, C.E., Röhl, U., Sugisaki, S., Tauxe, L., van de Flierdt, T., 2013. Reorganization of Southern Ocean plankton ecosystem at the onset of Antarctic glaciation. Science 340, 341–344. Ignatiades, L., 2012. Mixotrophic and heterotrophic dinoflagellates in eutrophic coastal waters of the Aegean Sea (eastern Mediterranean Sea). Bot. Mar. 55, 39–48. Jacobson, D.M., Anderson, D.M., 1986. Thecate heterotrophic dinoflagellates: feeding behaviour and mechanisms. J. Phycol. 22, 249–258. Jeong, H.J., Park, J.Y., Nho, J.H., Park, M.O., Ha, J.H., Seong, K.A., Jeng, C., Seong, C.N., Lee, K.Y., Yih, W.H., 2005. Feeding by the red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. microb. Ecol. 41, 131–143. Jeong, H.J., Seong, K.A., Yoo, Y.D., Kim, T.H., Kang, N.S., Kim, S., Park, J.Y., Kim, J.S., Kim, G.H., Song, J.Y., 2008. Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria. J. Eukaryot. microbiol. 55, 271–288. Jeong, H.J., Du Yoo, Y., Kim, J.S., Seong, K.A., Kang, N.S., Kim, T.H., 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45, 65–91. Kim, S.-Y., Moon, C.-H., Cho, H.-J., Lim, D.-I., 2009. Dinoflagellate cysts in coastal sediments as indicators of eutrophication: a case of Gwangyang Bay, South Sea of Korea. Estuar. Coasts 32 (6), 1225–1233. Kimor, B., Golandsky, B., 1977. Microplankton of the Gulf of Elat: aspects of seasonal and bathymetric distribution. Mar. Biol. 42, 55–67. Krepakevich, A., Pospelova, V., 2010. Tracing the influence of sewage discharge on coastal bays of Southern Vancouver Island (BC, Canada) using sedimentary records of phytoplankton. Cont. Shelf Res. 30, 1924–1940. Kumar, A., Patterson, R.T., 2002. Dinoflagellate cyst assemblages from Effingham Inlet, Vancouver Island, British Columbia, Canada. Palaeogeogr. Palaeoclimatol. Palaeoecol. 180, 187–206. Labiosa, R.G., Arrigo, K.R., Genin, A., Monismith, S.G., Van dijken, G., 2003. The interplay between upwelling and deep convective mixing in determining the seasonal phytoplankton dynamics in the Gulf of Aqaba: evidence from SeaWiFS and MODIS. Limnol. Oceanogr. 48, 2355–2368. Laiolo, L., Barausse, A., Dubinsky, Z., Palmeri, L., Goffredo, S., Kamenir, Y., Al-Najjar, T., Iluz, D., 2014. Phytoplankton dynamics in the Gulf of Aqaba (Eilat, Red Sea): a simulation study of mariculture effects. Mar. Pollut. Bull. 86 (1–2), 481–493. Lamy, F., Arz, H.W., Bond, G.C., Bahr, A., Pätzold, J., 2006. Multicentennial-scale hydrological changes in the Black Sea and northern Red Sea during the Holocene and the Arctic/North Atlantic oscillation. Paleoceanography 21, 1–11. Latasa, M., Landry, M.R., Schlüter, L., Bidigare, R.R., 1997. Pigment specific growth and grazing rates of phytoplankton in the central equatorial Pacific. Limnol. Oceanogr. 42, 289–298. Li, W.K.W., Zohary, T., Yacobi, Y.Z., Wood, A.M., 1993. Ultraphytoplankton in the eastern Mediterranean Sea: towards deriving phytoplankton from biomass flow cytometric measurements of abundance, fluorescence and light scatter. Mar. Ecol. Prog. Ser. 102, 79–87. Limoges, A., Londeix, L., de Vernal, A., 2013. Organic-walled dinoflagellate cyst distribution in the Gulf of Mexico. Mar. Micropaleontol. 102, 51–68. Lindell, D., Post, A.F., 1995. Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea. Limnol. Oceanogr. 40, 1130–1141. Madkour, F.F., El-Sherbiny, M.M., Aamer, M.A., 2010. Phytoplankton population along certain Egyptian coastal regions of the Red Sea. Egypt. J. Aquat. Biol. Fish. 14 (2), 95–109. Marret, F., Zonneveld, K.A.F., 2003. Atlas of modern organic-walled dinoflagellate cyst distribution. Rev. Palaeobot. Palynol. 125, 1–200. Mohamed, Z.A., Al-Shehri, A.M., 2011. Occurrence and germination of dinoflagellate cysts in surface sediments from the Red Sea off the coasts of Saudi Arabia. Oceanologia 53, 121–136. Morzadec-Kerfourn, M.T., Barros, A.M.A., Barros, A.B., 1990. Microfossiles à paroi organique et substances organiques des sédiments Holocènes de la lagune de Guarapina (Rio de Janeiro, Brésil). Bull. Centres Rech. Explor. Prod. ElfAquitaine 14, 575–582. Nassar, M.Z., Khairy, H.M., 2014. Checklist of phytoplankton species in the Egyptian waters of the Red Sea and some surrounding habitats (1990–2010). Annu. Res. Rev. Biol. 4 (23), 3566–3585. Nassar, M.Z., Mohamed, H.R., Khiray, H.M., Rashedy, S.H., 2014. Seasonal fluctuations of phytoplankton community and physico-chemical parameters of the north western part of the Red Sea, Egypt. Egypt. J. Aquat. Res. 40, 395–403. Ostenfeld, C.H., Schmidt, J., 1902. Plankton fra det Røde Hav of Adenbugten (Plankton from the Red Sea and the Gulf of Eden.). Vidensk. Medd. Dan. Naturhist. Foren. 1901, 141–182.

43

Pätzold, J., Abd El-Wahab Farah, O., Abu-Ouf, M., Al Hazmi, Y.M.M., Al-Roussan, S.A., Arz, H.W., Bagabas, K.A.A., Bassek, D., Blaschek, H., Böke, W., Donner, B., Edler, W., Felis, T., Gayed, H.Y.K., Gutowski, M., Hemleben, C., Hübner, A., Hübscher, C., Kadi, K.A., Kästner, R., Klauke, S., Körner, S.O., Kuhlmann, H., Lützeler, T., Meier, S., Melegy, M.M., Moammar, M.O., Zakari Mahomuda, A., Mokhtar, T.A., Moos, C., Omar, O.M., Rasheed, M., Rosiak, U., Salem, M., Schmidt, M., Schmitt, M., Stoffers, P., Shata, A.M., Themann, S., Weldeab, S., 1999. Report and preliminary results of METEOR cruise M44/3 Aqaba (Jordan)–Safga (Egypt)–Dubá (Saudi-Arabia)–Suez (Egypt)–Haifa (Israel). March 12–March 26–April 2–April 4, 1999. Berichte aus dem Fachbereich Geowissenschaften der Universität Bremen 194, pp. 1–135. Plaehn, O., Baschek, B., Badewien, T.H., Walter, M., Rhein, M., 2002. Importance of the Gulf of Aqaba for the formation of bottom water in the Red Sea. J. Geophys. Res. 107, 1–17. Pospelova, V., Kim, S.J., 2010. Dinoflagellate cysts in recent estuarine sediments from aquaculture sites of southern South Korea. Mar. Micropaleontol. 76, 37–51. Pospelova, V., Chmura, G.L., Boothman, W.S., Latimer, J.S., 2002. Dinoflagellate cyst records and human disturbance in two neighboring esturaries, New Bedford Harbor and Apponagansett Bay, Massachussetts (USA). Sci. Total Environ. 298, 81–102. Pospelova, V., Chmura, G.L., Walker, H.A., 2004. Environmental factors influencing the spatial distribution of dinoflagellate cyst assemblages in shallow lagoons of southern New England (USA). Rev. Palaeobot. Palynol. 128, 7–34. Pospelova, V., de Vernal, A., Pedersen, T.F., 2008. Distribution of dinoflagellate cysts in surface sediments from the northeastern Pacific Ocean (43–25°N) in relation to sea-surface temperature, salinity, productivity and coastal upwelling. Mar. Micropaleontol. 68, 21–48. Pospelova, V., Esenkulova, S., Johannessen, S.C., O'Brien, M.C., Macdonald, R.W., 2010. Organic-walled dinoflagellate cyst production, composition and flux from 1996 to 1998 in the central Strait of Georgia (BC, Canada): a sediment trap study. Mar. Micropaleontol. 75, 17–37. Post, A.F., Dedej, Z., Gottlieb, R., Li, H., Thomas, D.N., El-Absawi, M., El-Naggar, A., ElGharabawi, M., Sommer, U., 2002. Spatial and temporal distribution of Trichodesmium spp. in the stratified Gulf of Aqaba, Red Sea. Mar. Ecol. Prog. Ser. 239, 241–250. Price, A.M., Pospelova, V., 2011. High-resolution sediment trap study of organic-walled dinoflagellate cyst production and biogenic silica flux in Saanich Inlet (BC, Canada). Mar. Micropaleontol. 80, 18–43. Radi, T., de Vernal, A., 2008. Dinocysts as proxy of primary productivity in mid-high latitudes of the northern hemisphere. Mar. Micropaleontol. 68, 84–114. Radi, T., Pospelova, V., de Vernal, A., Barrie, J.V., 2007. Dinoflagellate cysts as indicators of water quality and productivity in British Columbia estuarine environments. Mar. Micropaleontol. 62, 269–297. Raitsos, D.E., Pradhan, Y., Brewin, R.J.W., Stenchikov, G., Hoteit, I., 2013. Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS One 8, e64909. http:// dx.doi.org/10.1371/journal.pone.006490 (1-9). Raven, J.A., 1986. Physiological consequences of extremely small size for autotrophic organisms in the sea. Can. Bull. Fish. Aquat. Sci. 214, l–70. Sætre, M.L.L., Dale, B., Abdullah, M.I., Sætre, G.-P., 1997. Dinoflagellate cysts as possible indicators of industrial pollution in a Norwegian fjord. Mar. Environ. Res. 44 (2), 167–189. Satta, C.T., Angles, S., Garces, E., Luglie, A., Padedda, B.M., Sechi, N., 2010. Dinoflagellate cysts in recent sediments from two semi-enclosed areas of the Western Mediterranean Sea subject to high human impact. Deep-Sea Res. II 57, 256–267. Shaikh, E.A., Roff, J.C., Dowidar, N.M., 1986. Phytoplankton ecology and production in the Red Sea off Jiddah, Saudi Arabia. Mar. Biol. 92, 405–416. Shin, H.H., Matsuoka, K., Yoon, Y.H., Kim, Y.O., 2010a. Response of dinoflagellate cyst assemblages to salinity changes in Yeoja Bay, Korea. Mar. Micropaleontol. 77, 15–24. Shin, H.H., Mizushima, K., Oh, S.J., Park, J.S., Noh, I.H., Iwataki, M., Matsuoka, K., Yoon, Y.H., 2010b. Reconstruction of historical nutrient levels in Korean and Japanese coastal areas based on dinoflagellate cyst assemblages. Mar. Pollut. Bull. 60, 1243–1258. Smeed, D.A., 2004. Exchange through Bab el Mandab. Deep-Sea Res. II 51, 455–474. Sofianos, S.S., Johns, W.E., 2003. An Oceanic Circulation Model (OGCM) investigation of the Red Sea circulation: 2. Three dimensional circulation in the Red Sea. J. Geophys. Res. 108 (C3), 1–5. http://dx.doi.org/10.1029/2001JC001185. Solignac, S., Grøsfjeld, K., Giraudeau, J., de Vernal, A., 2009. Distribution of recent dinocyst assemblages in the western Barents sea. Nor. J. Geol. 89, 109–119. Stambler, N., 2005. Bio-optical properties of the Northern Red Sea and the Gulf of Eilat (Aqaba) during winter 1999. J. Sea Res. 54, 186–203. Stockner, J.G., Antia, N.J., 1986. Algal picoplankton from marine and freshwater ecosystems: a multidisciplinary perspective. Can. Bull. Fish. Aquat. Sci. 43, 2472–2503. Taylor, F.J.R., Hoppenrath, M., Saldarriaga, J.F., 2008. Dinoflagellate diversity and distribution. Biodivers. Conserv. 17, 407–418. Ter Braak, C.J.F., Smilauer, P., 1998. Canoco reference manual and user's guide for Canoco for Windows. Software for Canonical Community Ordination (Version 4). Centre for Biometry, Wageningen. Usup, G., Ahmad, A., Matsuoka, K., Lim, P.T., Leaw, C.P., 2012. Biology, ecology and bloom dynamics of the toxic marine dinoflagellate Pyrodinium bahamense. Harmful Algae 14, 301–312. van der Plas, L., Tobi, A.C., 1965. A chart for judging the reliability of point counting results. Am. J. Sci. 263, 87–90. Vasquez-Bedoya, L.F., Radi, T., Ruiz-Fernandez, A.C., de Vernal, A., Machain-Castillo, M.L., Kielt, J.F., Hillaire-Marcel, C., 2008. Organic-walled dinoflagellate cysts and benthic foraminifera in coastal sediments of the last century from the Gulf of Tehuantepec, South. Pacific Coast of Mexico. Mar. Micropaleontol. 68, 49–65. Vink, A., Zonneveld, A.F., Willems, H., 2000. Organic-walled dinoflagellate cysts in western equatorial Atlantic surface sediments: distributions and their relation to environment. Rev. Palaeobot. Palynol. 112, 247–286. Wall, D., Dale, B., 1968. Modern dinoflagellate cysts and evolution of the Peridiniales. Micropaleontology 14 (3), 265–304.

44

R. Elshanawany, K.A.F. Zonneveld / Marine Micropaleontology 124 (2016) 29–44

Wall, D., Warren, J.S., 1969. Dinoflagellates in Red Sea piston cores. In: Degens, E.T., Ross, D.A. (Eds.), Hot Brines and Recent Heavy Metal Deposits in the Red Sea. Springer Verlag, Berlin, pp. 317–327. Weisse, T., 1989. The microbial loop in the Red Sea: dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar. Ecol. Prog. Ser. 55, 241–250. Yahel, G., Post, A.F., Fabricius, K., Marie, K.D., Vaulot, D., Genin, A., 1998. Phytoplankton distribution and grazing near coral reefs. Limnol. Oceanogr. 43, 551–563. Zonneveld, K.A.F., Brummer, G.J.A., 2000. Ecological significance, transport and preservation of organic-walled dinoflagellate cysts in the Somali Basin, NW Arabian Sea. Deep-Sea Res. II 47, 2229–2256. Zonneveld, K.A.F., Pospelova, V., 2015. A determination key for modern dinoflagellate cysts. Online. https://www.marum.de/dinocystkey.html. Zonneveld, K.A.F., Versteegh, G.J.M., Kodrans-Nsiah, M., 2008. Preservation and organic chemistry of Late Cenozoic organic-walled dinoflagellate cysts: a review. Mar. Micropaleontol. 86, 179–197. Zonneveld, K.A.F., Chen, L., Möbius, J., Mahmoud, M.S., 2009. Environmental significance of dinoflagellate cysts from the proximal part of the Po-river discharge plume (off southern Italy, Eastern Mediterranean). J. Sea Res. 62, 189–213.

Zonneveld, K.A.F., Susek, E., Fischer, G., 2010. Seasonal variability of the organic-walled dinoflagellate cyst production in the coastal upwelling region off Cape Blanc (Mauritania): a five-year survey. J. Phycol. 46, 202–215. Zonneveld, K.A., Chen, L., Elshanawany, R., Fischer, H.W., Hoins, M., Ibrahim, M.I., Pittauerova, D., Versteegh, G.J., 2012. The use of dinoflagellate cysts to separate human-induced from natural variability in the trophic state of the Po-river discharge plume over the last two centuries. Mar. Pollut. Bull. 64, 114–132. Zonneveld, K.A.F., Marret, F., Versteegh, G.J.M., Bogus, K., Bonnet, S., Bouimetarhan, I., Crouch, E., de Vernal, A., Elshanawany, R., Edwards, L., Esper, O., Forke, S., Grøsfjeld, K., Henry, M., Holzwarth, U., Kielt, J.F., Kim, S.Y., Ladouceur, S., Ledu, D., Chen, L., Limoges, A., Londeix, L., Lu, S.H., Mahmoud, M.S., Marino, G., Matsouka, K., Matthiessen, J., Mildenhal, D.C., Mudie, P., Neil, H.L., Pospelova, V., Qi, Y., Radi, T., Richerol, T., Rochon, A., Sangiorgi, F., Solignac, S., Turon, J.L., Verleye, T., Wang, Y., Wang, Z., Young, M., 2013. Atlas of modern dinoflagellate cyst distribution based on 2405 datapoints. Rev. Palaeobot. Palynol. 191, 1–198.