Taxonomy and distribution of benthic foraminifera in

Marine Micropaleontology 133 (2017) 1–20

Contents lists available at ScienceDirect

Marine Micropaleontology journal homepage: www.elsevier.com/locate/marmicro

Research paper

Taxonomy and distribution of benthic foraminifera in an intertidal zone of the Yellow Sea, PR China: Correlations with sediment temperature and salinity

MARK

Yanli Leia,f, Tiegang Lib,e,f,⁎, Zhimin Jianc, Rajiv Nigamd a

Department of Marine Organism Taxonomy & Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, PR China Key Laboratory of Marine Sedimentology and Environmental Geology, First Institute of Oceanography, SOA, Qingdao 266061, PR China c State Key Laboratory of Marine Geology, Tongji University, Shanghai 200092, PR China d Micropaleontology Laboratory, National Institute of Oceanography, Dona Paula, 403004, GOA, India e Laboratory for Marine Geology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266061, PR China f University of Chinese Academy of Sciences, Beijing 100049, PR China b

A R T I C L E I N F O

A B S T R A C T

Keywords: Benthic foraminifera Biodiversity Community dynamics Paleoenvironment Seasonal variation Tidal flat

Seasonal variations in foraminiferal populations from the intertidal environment of the Yellow Sea are not well known. This results in restricted understanding of environmental implications of foraminifera and their application in paleoenvironment reconstruction in this region. Community dynamics of both living and total (living plus dead) assemblages in a Qingdao intertidal flat were investigated from 2010 to 2012 during 17 months' sampling in two intertidal zones. Our study revealed a distinct seasonal variation in assemblages, which was more prominent in the low intertidal area. Foraminiferal abundance, species richness and Margalef index showed significant positive correlations to salinity, while species richness was negatively associated with temperature. A total of 52 species was identified and illustrated, including the dominant species: Ammonia beccarii, A. aomoriensis, A. aberdoveyensis, A. sobrina, Quinqueloculina seminula and Murrayinella globosa. Foraminiferal community parameters in the low intertidal area were higher than those in the high intertidal area, especially for the living assemblages, reflecting a seaward preference. Our study revealed that different tidal levels (low vs. high intertidal) had a more distinct influence in regulating foraminiferal assemblages than did seasonal influence.

1. Introduction Foraminifera are studied with the aim of establishing links between modern assemblages and environmental gradients that may be used as paleoenvironmental proxies (e.g., Nigam, 1986, 2005; Nigam et al., 2006; Papaspyrou et al., 2013; Manasa et al., 2016; Horton et al., 1999). In addition to their application in paleoceanographic studies, foraminifera play an important role in modern benthic ecology, being part of sediment-associated carbon and nitrogen cycles (Moodley et al., 2000; Mojtahid et al., 2011; van Oevelen et al., 2006). Benthic foraminifera sometimes dominate the microbenthic community (Alongi, 1992; Gooday et al., 1992), and especially in intertidal environments they may constitute 80% of total protozoan biomass (Lei et al., 2014). Since foraminifera are very sensitive to ambient environmental factors, they have been widely and successfully used to delimit marine or estuarine areas subjected to various natural and human-induced factors

⁎

(e.g., Murray, 1991; Hayward and Hollis, 1994; Sen Gupta, 1999; Debenay and Guillou, 2002; Gehrels and Haslett, 2002). Many studies have used intertidal foraminifera as precise biotic tools to develop high-resolution records of monsoon and relative sealevel changes (Scott and Medioli, 1978, 1980; Patterson, 1990; Jennings and Nelson, 1992; Jennings et al., 1995; Scott et al., 1996; Horton et al., 1999; Berkeley et al., 2007; Horton and Culver, 2008; Ghosh et al., 2009). Long-term studies on living benthic foraminifera in intertidal to shallow subtidal environments have been conducted mostly in the Atlantic region (Scott and Medioli, 1980; Lutze, 1968; Murray, 1983; Wefer, 1976; Murray and Alve, 2000; Alve and Murray, 2001), and only a few studies are known from the Pacific Ocean (Woodroffe et al., 2005). Similarly, such information is rare from the west Pacific region (Erskian and Lipps, 1987; Kitazato and Ohga, 1995), and no data are available from the seas around China. Paleoenvironmental reconstruction using foraminifera has been

Corresponding author at: First Institute of Oceanography, SOA, 266061 Qingdao, PR China. E-mail addresses: [email protected] (Y. Lei), tgli@fio.org.cn (T. Li).

http://dx.doi.org/10.1016/j.marmicro.2017.04.005 Received 3 June 2016; Received in revised form 24 April 2017; Accepted 30 April 2017 Available online 28 May 2017 0377-8398/ © 2017 Published by Elsevier B.V.


Y. Lei et al.

intertidal zone the sediment was muddy sand (GSM type), composed of 55.7% sand, 36.6% silt and 7.7% clay, with an average particle size of 3.844 μm. Grain size analysis was performed using a Laser Diffraction Particle Size Analyzer (Cilas 940L). During each sampling, environmental variables (salinity, air temperature, seawater temperature and sediment temperature) were measured in situ (Fig. 2). Temperature was measured by spirit thermometer (precision: 1 °C). Salinity was measured with a portable refractometer (precision: 1‰). Sediments were sampled using the Pushing-type Quantitative Layering Sampler with an inner diameter of 6 cm, giving a sampling surface of 28.26 cm2 (Lei et al., 2015). The top 1 cm of the sediment core was sliced and immediately fixed using 95% ethanol mixed with 1 g/L Rose Bengal so that live and dead specimens could be distinguished. Samples were then stored in a dark, cooling box and transported to the laboratory within 24 h. Fresh sediment with living foraminiferal specimens were collected simultaneously for taxonomic studies. In the laboratory, each sample was dried in an oven below 50 °C for 24 h and weighed and sieved through 0.150 mm and 0.063 mm meshes. The living and dead foraminiferal specimens were concentrated by an isopycnic separation technique using tetrachloromethane (D = 1.59) and the residues were also investigated (Jian et al., 1999).

widely carried out in China (e.g., Jian et al., 2001; Li et al., 2007, 2010). Background data such as species composition or distribution of foraminifera are essential for paleoenvironmental reconstruction from any region. The Qingdao intertidal area is a muddy sand intertidal flat, located in the bay mouth of the southern Yellow Sea. Lei and Li (2015) and Lei et al. (2016) studied the morphology and ecology of several Ammonia species in this area and documented the correlation between water depth and their distribution in the continental shelf sediments of the seas around China, and correlations between coiling direction or dimorphic forms and salinity or temperature. However, to our knowledge, no detailed data are available on the monthly variation in living benthic foraminifera in intertidal environments from the Yellow Sea. The lack of such information may hinder us from undertaking paleoenvironment reconstruction work in this region. Tracking short-term variations is important as these get compiled over years and influence long-term changes. This pioneering work of recording monthly variations for 17 months is a stepping stone to understanding long-term changes in more detail. Such studies will no doubt improve our approach to paleoenvironmental reconstruction. We investigated benthic foraminifera from the Qingdao intertidal flat in low and high intertidal areas from 2010 to 2012 during 17 months of sampling. We studied variations in living and total (living plus dead) foraminiferal assemblages (species composition, abundance, diversity and seasonal distribution) and environmental factors (temperature and salinity) and their possible interdependence. The main objectives of our work were to determine: (1) the species composition and diversity of foraminiferal fauna in this region, (2) whether there were seasonal variations in benthic foraminifera in the intertidal environment, (3) how the faunal dynamics were correlated to temperature and salinity, and (4) whether season or tidal level (low vs high intertidal area) controlled foraminiferal assemblages. Our results provide detailed background information on foraminiferal taxonomy and the ecological relationship of foraminifera to temperature and salinity in the intertidal environment of the Yellow Sea. This work will provide a detailed modern reference for paleoenvironmental studies of the Yellow Sea.

2.3. Classification and analyses Foraminiferal specimens were enumerated under a Nikon SSZ1500 stereomicroscope, with continuous zooming to a maximum amplification of 225×. Specimens were observed and photomicrographs taken. Foraminifera were identified to species level based on their morphological features using the respective original literature, some prevalent references (e.g., Loeblich and Tappan, 1987, 1994; Loeblich et al., 1992; Hayward et al., 2004, 2014), and the relevant regional taxonomic literature (e.g., Wang et al., 1988; Lei and Li, 2016). Individuals were picked and inventoried, and separated into two size fractions: large (> 0.150 mm) and small (0.063–0.150 mm). Because the small size group mainly comprised smaller specimens, juveniles or larvae of large foraminifera, and some small unidentified species, we decided to count and analyze only large foraminifera (> 0.150 mm) (Jian et al., 1999; Fontanier et al., 2002; Goineau et al., 2011; Lei et al., 2016). The small size group was only observed for comparison. In general, the whole sample was analyzed, but when foraminiferal density was too high, a riffle was used to subset samples with about 200–300 individuals examined from each sample. The total numbers of living and dead specimens picked from each sample are shown in Table 1. Living and total (living + dead) foraminiferal assemblages were studied separately for each sample. Foraminiferal abundance (individuals (ind.)/g dry weight (DW) of sediment), species richness (number of species/g DW of sediment), Margalef index (D) and Shannon–Wiener diversity (H′) were calculated. The Margalef index (D) was calculated as S-1/ln N, where S was the total number of species and N was the total number of individuals. The Shannon–Wiener index (H′) was calculated as -Σ Pi ln (Pi), where Pi was the proportion of total number of species made up of the ith species. Foraminiferal species occupying 5% or more of the total community abundance were regarded as dominant species.

2. Material and methods 2.1. Study area The study area was the intertidal zone of Qingdao Bay in the Yellow Sea (36°03′30″–36°03′42.00″N, 120°19′23″–120°19′25″E, Fig. 1). The Yellow Sea is a large inlet of the western Pacific Ocean lying between mainland China to the west and north and the Korean peninsula to the east. It is situated to the north of the East China Sea, which it bounds on a line running from the mouth of the Yangtze River to Cheju Island, South Korea. Qingdao has a long winter (from December to February) and represents a typical continental climate. Spring begins in March. The summer (from June to August) is influenced by the southeast monsoon and ocean currents, reflecting marine climate features. August is the warmest month (~ 25 °C) and January the coldest (approximately − 0.5 °C). The annual average temperature in this area is 12.7 °C. Since Qingdao is a coastal tourist city, its intertidal flat is affected by human activity, especially during August. 2.2. Sampling

2.4. Statistical analysis The sampling site, Qingdao Bay (Fig. 1), has a typical semidiurnal tide with a daily ebb and flow of about 6 h each. The tidal range is about 1.9–3.5 m. We collected samples over a period of 17 months from October 2010 to March 2012 from the low intertidal zone (QDL) and the high intertidal zone (QDH) when the tide ebbed. A total of 34 samples was collected and analyzed. The sediment in the low intertidal zone was sand (GSM type), composed of 96.9% sand, 2.4% silt and 0.8% clay, with an average particle size of 1.965 μm. In the high

Simple nonparametric Spearman correlation was used to evaluate the relationship between biotic parameters (abundance, species richness, Margalef and Shannon–Wiener diversity indices) and the environmental variables (air temperature, sediment temperature, seawater temperature and salinity). These analyses were performed using the Statistical Package for the Social Sciences (SPSS, version 15.0). Data were log (x + 1) transformed to meet the assumptions of normality and 2


Y. Lei et al.

Fig. 1. Location map of the Qingdao intertidal flat, the Yellow Sea. The sampling site is indicated by an open square.

Fig. 2. Variations of temperature (A) and salinity (B) during monthly samplings from October 2010 to February 2012.

Table 1 The total numbers of living and dead specimens picked from each sample. Low intertidal area

Living specimens

Dead specimens

High intertidal area

Living specimens

Dead specimens

2010-10-22QDL 2010-11-23QDL 2010-12-23QDL 2011-01-22QDL 2011-02-28QDL 2011-03-20QDL 2011-04-18QDL 2011-05-17QDL 2011-06-13QDL 2011-07-05QDL 2011-08-30QDL 2011-09-29QDL 2011-10-29QDL 2011-11-28QDL 2011-12-26QDL 2012-01-12QDL 2012-02-10QDL

54 95 68 68 184 116 143 124 73 119 145 34 121 310 379 339 265

37 10 37 54 233 138 92 236 247 73 138 10 34 82 180 196 150

2010-10-22QDH 2010-11-23QDH 2010-12-23QDH 2011-01-22QDH 2011-02-28QDH 2011-03-20QDH 2011-04-18QDH 2011-05-17QDH 2011-06-13QDH 2011-07-05QDH 2011-08-30QDH 2011-09-29QDH 2011-10-29QDH 2011-11-28QDH 2011-12-26QDH 2012-01-12QDH 2012-02-10QDH

41 54 90 100 146 31 122 95 29 58 19 87 14 70 61 43 90

134 153 218 233 111 270 255 71 371 231 163 235 61 466 367 199 417

3


Y. Lei et al.

Fig. 3. Variations of abundance of foraminiferal assemblages in the low intertidal area (A) and high intertidal area (B) during monthly samplings from October 2010 to February 2012.

February 2011 and January 2012. The total foraminiferal abundance varied from 6 to 112 ind./g DW of sediment (mean value: 36.35 ind./g DW of sediment). In 2011 the peak of total abundance occurred in February (52 ind./g DW of sediment), and it later decreased. In September 2011, it reached its lowest value (6 ind./g DW of sediment). In 2012, the highest total abundance was 112 ind./g DW of sediment in January, and it later decreased again. The living foraminiferal trend follows the total foraminiferal assemblage pattern, with higher abundance occurring in the winter season (Fig. 3A). The living foraminiferal abundance ranged between 4 and 71 ind./g DW of sediment (mean value: 21.24 ind./g DW of sediment). In 2011 the peak of living foraminiferal abundance occurred in February (23 ind./g DW of sediment). It later decreased gradually until the lowest value of 4 ind./g DW of sediment was reached in September. In 2012 the highest living foraminiferal abundance reached 71 ind./g DW of sediment in January, and afterwards decreased again. In January and February, many juvenile living foraminiferal species could be observed under the microscope based on our taxonomic observations. The growth rate in 2011–2012 was probably higher than in the previous winter. Foraminiferal abundance matched well with salinity (Figs. 2 and 3), suggesting that seasonality was greatly affected by salinity.

homogeneity of variances. To examine the monthly variation in community parameters, Cluster analysis using Bray–Curtis similarity matrices was performed in the PRIMER v6.1 package (Clarke and Gorley, 2006). Clusters were differentiated using the CLUSTER procedure. 3. Results 3.1. Environmental variables During the sampling period in the Qingdao intertidal flat, the air temperature ranged from 1.5 to 26.5 °C, seawater temperature ranged from 4 to 26.1 °C and sediment temperature ranged from 3 to 24.9 °C. The temperatures of the air, seawater and sediment showed a similar trend, with the lowest value occurring in January 2011 and the highest in August 2011 (Fig. 2). After August, the temperature gradually dropped and finally reached its lowest value in January 2012. The variation in salinity showed a reverse trend to the temperature, ranging from 31‰ to 38‰ and reflecting a characteristic of winter high and summer low (Fig. 2). In the first year, 2011, salinity reached the highest value in January and decreased from March until August. It later increased and reached its highest value in winter (Fig. 2).

3.2.2. High intertidal area In this area, the abundance of the total foraminiferal assemblage was on average 38.35 ind./g DW of sediment (Fig. 3B), but it varied from 9 ind./g DW of sediment (in October 2011) to 76 ind./g DW of sediment (in February 2012). The first peak occurred in April 2011,

3.2. Foraminiferal abundance 3.2.1. Low intertidal area Total foraminifera showed a distinctly seasonal dynamic (Fig. 3A), with the highest value occurring only in the winter season, i.e.,

Fig. 4. Variations of species richness of foraminiferal assemblages in the low intertidal area (A) and high intertidal area (B) during monthly samplings from October 2010 to February 2012.

4


Y. Lei et al.

Fig. 5. Variations of Margalef index (D) of foraminiferal assemblages in the low intertidal area (A) and high intertidal area (B) during monthly samplings from October 2010 to February 2012.

after which total abundance fluctuated several times before reaching a second peak in November 2011. However, unlike the low intertidal area, there was no distinct seasonal pattern in the abundance of total foraminifera. The living foraminifera did not show a clear seasonal pattern (Fig. 3B), and nor did the variation in living foraminifera match that of the total assemblage. Living abundance was on average 8.65 ind./g DW of sediment, ranging from 2 to 18 ind./g DW of sediment. The highest living abundance occurred in February 2011 and the lowest in August 2011. It is possible that the seasonal signature in this area is impeded by high wave energy, which allows few foraminifera to survive. A study of the sediment might help to resolve this.

living foraminifera was 10.94, ranging from four (December 2011) to 22 (November 2011).

3.3. Foraminiferal species richness

3.4. Foraminiferal Margalef index (D)

3.3.1. Low intertidal area Like the abundance, seasonality is prominent in species richness of total foraminifera (Fig. 4A). Two peaks were observed per year, occurring in spring (February 2011) and autumn (December 2011). The species richness of total foraminifera was on average 14.94 and varied from seven (July 2011) to 30 (December 2011). The features of species richness of living foraminifera resembled those of the total assemblage (Fig. 4A). The average species richness of

3.4.1. Low intertidal area The Margalef index for total and living foraminiferal assemblages showed a seasonal influence, with two peaks occurring per year (Fig. 5A). The index was high in spring and autumn but low in summer and winter. The mean value of the Margalef index for total foraminifera was 4.04, ranging from 1.88 (July 2011) to 6.93 (November 2011). The mean value for living foraminifera was 3.42, varying between 1.40 (December 2011) and 5.74 (November 2011).

3.3.2. High intertidal area The species richness of total and living foraminifera did not show a distinct seasonal pattern in the high intertidal area (Fig. 4B). The species richness of total foraminifera was on average 10.47, varying from a high of 17 in April 2011 to a low of six in October 2011; and that of living foraminifera was 8.65, fluctuating from a high of 10 (in April 2011) to a low of two (in August 2011). No correspondence was found between the patterns of total and living foraminifera (Fig. 4B).

Fig. 6. Variations of Shannon-Wiener index (H′) of foraminiferal assemblages in the low intertidal area (A) and high intertidal area (B) during monthly samplings from October 2010 to February 2012.

5


Y. Lei et al.

in the high intertidal area included A. beccarii, A. aomoriensis and Q. seminula, constituting on average 34.33%, 32.11% and 10.43%, respectively (Fig. 8C). The living fauna in this area was also dominated by A. beccarii, A. aomoriensis and Q. seminula, but their proportions were different, being 26.31%, 37.42%, and 18.61%, respectively (Fig. 8D). In addition, M. globosa and A. aberdoveyensis? were also abundant, making up on average 5% of the total or living foraminiferal abundance. The dominant species in low and high intertidal areas are shown in Fig. 9. Different species showed different patterns. The dominant species showed a seasonal character in the low intertidal area, both for living and for total assemblages. For instance, A. aomoriensis and A. beccarii had a similar dynamic pattern with only one peak annually. Trochammina inflata peaked only once a year, in autumn. Quinqueloculina seminula exhibited two peaks per year in the low intertidal area, in the summer and winter seasons. Living M. globosa increased several times except in the summer season (Fig. 9). In contrast, in the high intertidal area, the seasonal pattern for all species was not so distinct. Even T. inflata was not present in the high intertidal area (Fig. 9).

3.4.2. High intertidal area The variation in the Margalef index for total foraminifera did not show a distinct seasonal pattern (Fig. 5B). The mean value of the Margalef index was 2.64 across all the samplings, but varied from a low of 1.93 (in March 2011) to a high of 4.15 (in April 2011). The dynamic of the Margalef index for living foraminifera neither showed a seasonal pattern nor matched that of the total assemblage (Fig. 5B). The mean value was 2.77 across all samplings, ranging from a high of 5.60 (in October 2011) to a low of 1.47 (in December 2011). The Margalef index tended to match the species richness for total and living foraminifera in both the low and the high intertidal areas. 3.5. Foraminiferal Shannon–Wiener diversity (H′) 3.5.1. Low intertidal area Shannon–Wiener diversity for total foraminifera showed a distinctly seasonal variation, and two peaks were observed per year (Fig. 6A). The mean value of the Shannon–Wiener index for total foraminifera was 1.75, but it varied from 1.15 (December 2010) to 2.33 (November 2011). The first peak occurred in January 2011, and then it decreased, with its lowest value in summer (July 2011). It later increased, and reached a second peak in November 2011. The dynamic of the Shannon–Wiener diversity of living foraminifera was similar to that of the total assemblage (Fig. 6A). The mean value was 1.59, ranging from a low of 0.88 (December 2010) to a high of 2.20 (November 2011).

3.7. Correlations between foraminifera and environmental factors We conducted Spearman's correlation analysis between foraminiferal community parameters (abundance, species richness, Margalef index and Shannon–Wiener diversity) and environmental variables (Table 2). Statistical analysis showed that correlations between biotic and abiotic variables in the low intertidal area were more significant than those in the high intertidal area. For example, in the low intertidal zone, the abundance, species richness and Margalef index were all significantly positively correlated to salinity; and species richness was negatively correlated to temperature (Table 2). In contrast, in the high intertidal zone, only abundance was significantly associated with salinity and correlated with temperature. Other biotic parameters did not show any correlation with environmental variables (Table 2). We also conducted Spearman's correlation analysis between individual species and environmental variables (Table 3). In the low intertidal zone, the abundances of 10 living foraminiferal species: Ammoglobigerina globigeriniformis, Q. argunica, Q. subungeriana, Buccella frigida, Pararotalia armata, Ammonia aomoriensis, A. beccarii, A. pauciloculata, Elphidium incertum and E. macellum, were significantly positively correlated with salinity. In addition, A. globigeriniformis, Q. subungeriana, B. frigida and A. beccarii were negatively correlated with temperature. In contrast, in the high intertidal area, the correlations between species and environmental variables were not as significant as those in the low intertidal area. Only four species showed correlation with environmental factors, but the tendency was the same. For instance, Q. seminula and A. aomoriensis were positively correlated with salinity while A. globigeriniformis and A. aomoriensis were negatively correlated with temperature (Table 3).

3.5.2. High intertidal area The Shannon–Wiener diversity of total foraminifera did not show a distinct seasonal pattern (Fig. 6B). The mean value was 1.52, but it varied from a low of 1.13 in October 2010 to a high of 1.85 in April 2011. Similarly, the diversity of living foraminifera neither showed a distinct seasonal pattern nor matched that of the total assemblage (Fig. 6B). The mean value of living Shannon–Wiener diversity was 1.32, fluctuating from 1.90 (in July 2011) to 1.04 (in August and December 2011). 3.6. Species composition A total of 52 benthic foraminiferal species was identified and illustrated in Plates 1–7. They belonged to three orders, 15 families and 28 genera (Appendix). Living specimens were stained by Rose Bengal. In the low intertidal area, the total foraminiferal fauna was composed of 84.96% Rotaliida, 10.97% Miliolida and 4.07% Textulariida (Fig. 7). In the high intertidal area, the total fauna comprised 88.57% Rotaliida, 10.61% Miliolida and 0.82% Textulariida; that is, the proportion of Rotaliida increased but Textulariida decreased (Fig. 7). The dominant species of total foraminiferal fauna in the low tidal area included Ammonia beccarii, A. aomoriensis, A. aberdoveyensis? and Quinqueloculina seminula, representing on average 42.80%, 11.64%, 10.66% and 10.43%, respectively (Fig. 8A). For the living fauna, the composition of dominant species was similar to that of the total fauna; that is, A. aomoriensis, A. beccarii and Q. seminula accounted for – on average – 37.42%, 26.31% and 18%, respectively (Fig. 8B). In addition, Murrayinella globosa was also common, representing on average 6.21% of the total abundance and 5.24% of the living foraminiferal abundance. Ammonia sobrina and Trochammina inflata were not very common but they occasionally made up certain proportions (e.g., A. sobrina accounted for about 23% in September 2011) of the total foraminiferal abundance in low intertidal area. In September 2011 the total number of foraminiferal specimens was low (Fig. 8A, B, Table 1). In the high intertidal area, species composition was relatively simpler than in the low intertidal area. The dominant species of total fauna

3.8. Cluster analyses across all sampling seasons and tidal areas To detect the importance of season and sea level (low vs high intertidal area) in regulating foraminiferal community parameters, cluster analyses were carried out (Figs. 10–13). These dendrograms were computed using Euclidean distance foraminiferal community parameter data by log (x + 1) transformation. The abundance cluster analysis based on total foraminifera resulted in 34 foraminiferal assemblages falling into two clades at 80% similarity level (Fig. 10A): clade 1 of mainly low intertidal assemblages; and clade 2 of assemblages of mixed seasons and tidal levels (low vs. high intertidal). Living abundance cluster analysis grouped foraminifer samples into three clades (Fig. 10B): clade 1 mainly of high intertidal

6


Y. Lei et al.

Plate 1. Micrographs of benthic foraminifera in the Qingdao intertidal flat of the Yellow Sea. Scale bars = 200 μm. 1, Reophax curtus Cushman, 1920. 2, Ammobaculites agglutinans (d'Orbigny, 1846). 3, Ammoglobigerina globigeriniformis (Park & Jones, 1865). 4, Trochammina squamata Jones & Parker, 1860. 5, Trochammina astrifica Rhumbler, 1938. 6, Trochammina inflata (Montagu, 1808). 7, Arenoparrella asiatica Polski, 1959.

foraminiferal communities into three clades (Fig. 11B): clade 1 of foraminiferal assemblages with mixed seasons and tidal areas; clade 2 of mainly high intertidal assemblages; and clade 3 of low intertidal assemblages mostly from the winter season. Total Margalef index cluster analysis grouped 34 foraminiferal communities into two clades at 90% similarity level (Fig. 12A): clade 1 of mainly low intertidal assemblages; clade 2 of communities mostly of the high intertidal assemblages with mixed seasons. Living Margalef

assemblages; clade 2 with assemblages of mixed seasons and tidal levels; and clade 3 included three winter assemblages from the low intertidal area. Total species richness cluster analysis grouped the 34 foraminiferal assemblages into two clades at 90% similarity level (Fig. 11A): clade 1 of mostly high intertidal assemblages with mixed seasons and tidal areas; and clade 2 included basically low intertidal assemblages but with mixed seasons. Living species richness cluster analysis grouped 34

7


Y. Lei et al.

Plate 2. Continued. Scale bars = 200 μm. 8, Pseudoclavulina juncea Cushman, 1936. 9, Spiroloculina jucunda Cushman & Ellisor, 1944. 10, Spiroloculina communis Cushman & Todd, 1944. 11, Massilina secans (d'Orbigny, 1826). 12, Quinqueloculina seminula (Linnaeus, 1758). 13, Quinqueloculina subungeriana Serova, 1960.

with mixed seasons; and clade 2 of assemblages mainly from the high intertidal but with mixed seasons. Living Shannon–Wiener diversity cluster analysis also grouped foraminiferal assemblages into two clades (Fig. 13B): clade 1 mostly of assemblages from the high intertidal across different seasons; and clade 2 of assemblages mainly from the low intertidal but with mixed seasons.

index cluster analysis also grouped foraminiferal communities into three clades (Fig. 12B): clade 1 of assemblages from mixed seasons and mixed tidal areas; clade 2 of mainly high intertidal communities; and clade 3 includes mainly low intertidal assemblages. Total Shannon–Wiener diversity cluster analysis grouped 34 foraminiferal assemblages into two clades at 90% similarity level (Fig. 13A): clade 1 of assemblages mainly from the low intertidal but

8


Y. Lei et al.

Plate 3. Continued. Scale bars = 200 μm. 14, Quinqueloculina argunica (Gerke, 1938). 15, Triloculina cf. affinis d'Orbigny, 1852. 16, Triloculina sommeri Tinoco, 1955. 17, Rosalina bradyi (Cushman, 1915). 18, Rosalina vilardeboana d'Orbigny, 1839. 19, Discorbinella subcomplanata (Parr, 1950).

4. Discussion

studies, for example on the Great Barrier Reef shelf and north Queensland, Australia (Woodroffe et al., 2005; Berkeley et al., 2008), Vendée in western France (Debenay et al., 2006), the south and west coasts of the UK (Horton et al., 1999), North Carolina, USA (Horton and Culver, 2008), and the southwestern Baltic Sea and the Gulf of Cambay (Ghosh et al., 2009). In different regions of the intertidal environments, the Rotaliida group usually makes up the highest proportions, followed by Miliolida and then by Textulariida. The dominant species showed distinct seasonality in the low

4.1. Foraminiferal species composition In the present study, total foraminiferal fauna in the low intertidal area includes 84.96% Rotaliida, 10.97% Miliolida and 4.07% Textulariida; while in the high intertidal area, the proportion of Rotaliida is 88.57%, Textulariida decreases to 0.82% and only Miliolida remains unchanged (10.61%). Our results agree with some previous

9


Y. Lei et al.

Plate 4. Continued. Scale bars = 200 μm. 20, Rosalina floridana (Cushman, 1922). 21, Murrayinella globosa (Millet, 1903). 22, Planoglabratella opercularis (d'Orbigny, 1826). 23, Cibicidoides pseudoungeriana (Cushman, 1922). 24, Haynesina depressula (Walker & Jacob, 1798). 25, Haynesina depressula simplex (Cushman, 1933). 26, Protelphidium glabrum (Ho, Hu & Wang, 1965). 27, Nonionella stella Cushman & Moyer, 1930. 28, Melonis affinis (Reuss, 1851).

dominated in autumn, spring and summer (Murray, 1968). Nevertheless, other studies carried out in different intertidal environments in varied locations reported different dominant species (Woodroffe et al., 2005; Berkeley et al., 2008; Debenay et al., 2006; Horton et al., 1999; Horton and Culver, 2008), such as Ammonia spp., Tochammina inflata, Quinqueloculina spp., Murrayinella globosa (= Shackoinella globosa). These species were also found frequently in our study. Many studies have successfully reconstructed sea-level changes

intertidal area, although different species showed different patterns. For instance, Q. seminula had two peaks per year (in the summer and winter), while M. globosa increased several times except in the summer. Ammonia aomoriensis and A. beccarii, however, had only one peak per year (in the winter season). This result agrees with Murray (1968, 1992), who suggested that seasonal abundance of different species might be different. In a brackish lagoon of Christchurch harbor (New Zealand) Haynesina dominated in the winter, while Elphidium

10


Y. Lei et al.

Plate 5. Continued. Scale bars = 200 μm. 29, Buccella frigida (Cushman, 1922). 30, Pseudoeponides japonicus Uchio, 1950. 31, Pararotalia armata (d'Orbigny, 1826). 32, Ammonia beccarii (Linnaeus, 1758). 33, Ammonia aomoriensis (Asano, 1951). 34, Ammonia aberdoveyensis Haynes, 1973. 35, Ammonia pauciloculata (Phleger & Parker, 1951). 36, Ammonia tepida (Cushman, 1926).

and M. globosa were mostly dominant throughout the year in the Qingdao intertidal flat. Foraminifera in fossil cores might be used as bioindicators to reconstruct sea-level changes in the intertidal environment of the Yellow Sea. Species identification for this study was based on morphological characteristics, so some cryptic species may have been overlooked, for instance, the thecate Monothalamids (Pawlowski et al., 2013). Introduction of multiple techniques such as molecular protocols would

based on information about dominant species. Horton et al. (1999) demonstrated that sea-level changes could be reconstructed by the vertical distribution of intertidal foraminiferal biofacies in a UK intertidal flat. Woodroffe et al. (2005) studied intertidal foraminifera from mangroves of the central Great Barrier Reef, Australia, and reconstructed sea-level changes using foraminiferal species composition. Similar work is also known from the Indian Ocean (Ghosh et al., 2009). In our study, A. beccarii, A. aomoriensis, A. aberdoveyensis?, Q. seminula

11


Y. Lei et al.

Plate 6. Continued. Scale bars = 200 μm. 37, Ammonia sobrina (Shupack, 1934). 38, Ammonia maruhasii (Kuwano, 1950). 39, Rotalinoides compressiuscula (Brady, 1884). 40, Rotalidium annectens (Parker & Jones, 1865). 41, Cribrononion gnythosuturatum Ho, Hu et Wang, 1965. 42, Cribroelphidium magellanicum (Heron-Allen & Earland, 1932). 43, Cribroelphidium incertum Williamson, 1858. 44, Elphidium advenum (Cushman, 1922).

maintained to the greatest possible extent. In this work, only the large foraminiferal group (> 150 μm) was analyzed, relatively small species such as Rosalina floridana (size: 100 μm × 85 μm × 50 μm) were also observed (see Appendix). We compared the small size group (63–150 μm), which mainly comprised smaller or juvenile species occurring in the large group, as well as some unknown larvae or uncertain individuals. Since the sampling had been intensive (i.e., 17 months) in this tidal flat, we surmise that the

improve detection of potential species diversity (e.g., Hayward et al., 2004; Pawlowski, 2000; Pawlowski et al., 2013). Considering that one of the most important applications of foraminifera lies in using their fossil morphology to compare biostratigraphy and to reconstruct the paleoenvironment, their morphological taxonomy will always be important. Therefore, we advocate that future molecular protocols act as links to connect morphology and genetic results. It is preferable that traditional taxonomy based on morphology at the species level is

12


Y. Lei et al.

Plate 7. Continued. Scale bars = 200 μm. 45, Elphidium macellum (Fichtel & Moll, 1798). 46, Elphidium limpidum Ho, Hu & Wang, 1965. 47, Elphidium excavatum (Terquem, 1875). 48, Elphidium clavatum Cushman, 1930. 49, Elphidium incertum (Williamson, 1858). 50, Elphidium crispum (Linnaeus, 1758). 51, Elphidium jenseni (Cushman, 1924). 52, Elphidium hispidulum Cushman, 1936.

America (Williams, 1989; Scott et al., 1996); and from Atlantic seaboard of Europe (Le Campion, 1970; Phleger, 1970; Pujos, 1976; Murray, 1991). Murray and Alve (2000) summarized studies based on monthly sampling from intertidal to shallow subtidal environments worldwide. No similar studies have so far been carried out in Chinese seas in the west Pacific region (Erskian and Lipps, 1987; Kitazato and Ohga, 1995). Our study, therefore, provides first-hand data on the abundance of benthic foraminifera; it also includes a taxonomic survey and considers the environmental implications for the local region. Our result revealed distinct seasonal variations of foraminiferal assemblages in the intertidal flat environment, especially in the low

diversity obtained in the present study represents a relatively comprehensive list of the commonly seen species (> 150 μm fraction) for this area. 4.2. Seasonal variation of foraminiferal community parameters Previous benthic foraminiferal investigations have largely been carried out from the Atlantic Ocean region (Scott and Medioli, 1978, 1980; Coles and Funnell, 1981; Smith et al., 1984; Gehrels, 1994; de Rijk, 1995; de Rijk and Troelstra, 1997; Boomer, 1998; Horton et al., 1999; Murray and Alve, 2000); some were from Pacific coasts of North 13


Y. Lei et al.

Fig. 7. Percent composition of foraminiferal abundance based on total assemblages at order level in the low and high intertidal areas.

occurring in spring and autumn and low values in summer and winter. When we compared the foraminiferal community parameters between different intertidal areas, we found almost all of the parameters in the low intertidal area were higher than those in the high intertidal area,

intertidal area. The foraminiferal abundance exhibited a seasonal variation, with high values occurring during winter. Other community parameters – including species richness, Margalef index and Shannon–Wiener diversity – showed a variation with high values

Fig. 8. Proportional abundance of different dominant species in the low intertidal area (A–B) and high intertidal area (C–D). A, C, total foraminiferal assemblages. B, D, living foraminiferal assemblages.

14


Y. Lei et al.

Fig. 9. Variations of dominant species (Trochammina inflata, Quinqueloculina seminula, Murrayinella globosa, Ammonia aomoriensis, Ammonia beccarii) in different intertidal areas.

4.3. Linkage between foraminifera and environmental factors

especially for the living foraminiferal assemblages. The only exception was the total abundance, which from the low intertidal area was slighter lower than from the high intertidal area. This can be easily explained by the movement effects of fossils, which can be transported by tidal activity from the low to the high intertidal area. The seasonal changes in foraminiferal density may be caused by many factors including variations in food supply, rate of reproduction and survival of juveniles (Murray, 1992). Therefore, foraminiferal reproduction peaks may occur once or twice a year, or several times a year (Alve and Murray, 2001). We should mention that 18 out of 34 samples had < 300 specimens (e.g., October and November 2010; July and August 2011), at that time both low and high intertidal area had very low foraminiferal abundances. In addition, the lack of replication might be a shortcoming of this study, further comparison with different studies should consider the possible patchiness of benthic foraminiferal communities (Buzas et al., 2015).

The intertidal zone of the marine system is highly variable in terms of environmental parameters (Magno et al., 2012). Seasonal variation in benthic foraminifera can be controlled by several biotic and abiotic factors, such as sediment texture and grain size (e.g., Magno et al., 2012), bottom currents and seasonal food supply (e.g., Diz et al., 2004) and organic matter exporting (e.g., Fontanier et al., 2002). Despite the complex spatial and temporal patterns of environmental characteristics in relation to seasonal and tidal cycles in the intertidal zone, few studies are concerned with the seasonal changes in foraminifera and the relationships between these changes and environmental factors (Debenay et al., 2006). In our study, Spearman's correlation analyses revealed a close correlation between foraminifera and temperature and/or salinity, especially salinity. In the low intertidal zone, foraminiferal abundance, species richness and Margalef index were all significantly positively correlated to salinity. Only species richness was negatively correlated to temperature (Table 2). Horton et al. (1999) proposed the development 15


Y. Lei et al.

Table 2 Correlations (Spearman's r values) between foraminiferal community parameters and environmental factors. Data were based on the data after log (x + 1) transformed from 17 months of sampling. The α-level is 0.05. p-values (in the parentheses) beneath 0.05 and 0.01 are marked by a single asterisk, respectively, and double asterisks. Community parameters Low intertidal area Abundance (N) Species richness (S) Margalef index (D) Shannon-Wiener index (H′) High intertidal area Abundance (N) Species richness (S) Margalef index (D) Shannon-Wiener index (H′)

Sediment temperature

Water temperature

Salinity

Total Living Total Living Total Living Total Living

− 0.434 (0.082) − 0.435 (0.081) − 0.503 (0.039)* − 0.410 (0.102) − 0.369 (0.145) − 0.250 (0.334) − 0.207 (0.426) − 0.179 (0.491)

− 0.407 (0.105) − 0.401 (0.111) − 0.490 (0.046)* − 0.407 (0.105) − 0.374 (0.139) − 0.263 (0.309) − 0.218 (0.400) − 0.196 (0.450)

0.519 (0.033)⁎ 0.519 (0.033)⁎ 0.617 (0.008)** 0.582 (0.014)⁎ 0.554 (0.021)⁎ 0.468 (0.058) 0.315 (0.219) 0.336 (0.187)


− 0.316 (0.217) − 0.571 (0.017)⁎ − 0.278 (0.280) − 0.379 (0.133) − 0.071 (0.786) 0.210 (0.418) 0.043 (0.870) − 0.354 (0.163)

− 0.294 (0.251) − 0.536 (0.019*) − 0.258 (0.318) − 0.421 (0.092) − 0.039 (0.881) 0.125 (0.632) 0.049 (0.852) − 0.429 (0.085)

0.485 (0.048)⁎ 0.549 (0.022)⁎ 0.241 (0.352) 0.277 (0.282) − 0.021 (0.935) − 0.305 (0.235) − 0.115 (0.659) 0.290 (0.260)

Table 3 Correlations (Spearman's r values) between individual species and environmental factors. Data were based on the data after log (x + 1) transformed from 17 months of sampling. The αlevel is 0.05. p-values (in the parentheses) beneath 0.05 and 0.01 are marked by a single asterisk, respectively, and double asterisks. Dominant species Low intertidal area Ammoglobigerina globigeriniformis (Park & Jones, 1865) Quinqueloculina argunica (Gerke, 1938) Quinqueloculina subungeriana Serova, 1960 Buccella frigida (Cushman, 1922) Pararotalia armata (d'Orbigny, 1826) Ammonia aomoriensis (Asano, 1951) Ammonia beccarii (Linnaeus, 1758) Ammonia pauciloculata (Phleger & Parker, 1951) Elphidium incertum (Williamson, 1858) Elphidium macellum (Fichtel & Moll, 1798) High intertidal area Ammoglobigerina globigeriniformis (Park & Jones, 1865) Ammonia aomoriensis (Asano, 1951) Ammonia beccarii (Linnaeus, 1758) Quinqueloculina seminula (Linnaeus, 1758)

Sediment temperature

Water temperature

Salinity

Total Living Total Living Total Living Total Living Total Living Total Living Total Living Total Living Total Living Total Living

− 0.548 (0.023)* − 0.518 (0.033)* − 0.299 (0.244) – − 0.470 (0.057) − 0.294 (0.252) − 0.517 (0.033)* − 0.466 (0.060) − 0.323 (0.206) − 0.299 (0.244) − 0.317 (0.216) − 0.487 (0.047)* − 0.452 (0.068) − 0.554 (0.021)* − 0.316 (0.217) – − 0.476 (0.054) − 0.420 (0.093) − 0.354 (0.164) − 0.378 (0.134)

−0.500 (0.041)* −0.485 (0.049)* −0.280 (0.277) – −0.497 (0.042)* −0.309 (0.228) −0.483 (0.050)* −0.428 (0.087) −0.326 (0.201) −0.282 (0.274) −0.301 (0.241) −0.469 (0.058) −0.420 (0.094) −0.517 (0.034)* −0.237 (0.361) – −0.531 (0.028)* −0.496 (0.043)* −0.318 (0.213) −0.375 (0.138)

0.551 (0.022)* 0.546 (0.023)* 0.572 (0.016)* – 0.570 (0.017)* 0.481 (0.051) 0.604 (0.010)* 0.518 (0.033)* 0.572 (0.017)* 0.530 (0.029)* 0.381 (0.131) 0.572 (0.016)* 0.540 (0.025)* 0.671 (0.003)** 0.515 (0.034)* – 0.546 (0.023)* 0.367 (0.147) 0.448 (0.072) 0.534 (0.027)*


− 0.320 (0.210) − 0.505 (0.039)* − 0.321 (0.208) − 0.503 (0.040)* − 0.334 (0.190) − 0.290 (0.260) − 0.285 (0.268) − 0.423 (0.090)

−0.315 (0.218) −0.492 (0.045)* −0.315 (0.219) −0.531 (0.028)* −0.316 (0.216) −0.273 (0.289) −0.233 (0.369) −0.387 (0.124)

0.302 (0.238) 0.345 (0.175) 0.462 (0.062) 0.530 (0.029) 0.502 (0.040)* 0.188 (0.469) 0.434 (0.082) 0.519 (0.033)*

4.4. Are foraminifera regulated by different seasons or by different tidal areas?

of a relationship between a foraminiferal assemblage and environmental factors to obtain a transfer function or biotic index. Based on our results, three biotic indices, abundance (N), species richness (S) and Margalef index (D), could be potentially used for this calculation (Table 2). With the exception of the community parameters, some dominant species (e.g., Q. subungeriana and A. aomoriensis) were positively correlated to salinity, or negatively to temperature. The relationships reflected by the dominant species (e.g., A. aomoriensis and A. beccarii) could also be used for the calculation (Lei and Li, 2015; Lei et al., 2016).

Is the season or the tidal area (low vs high intertidal area) more important for regulating foraminiferal community parameters? To answer this question, a series of cluster analyses were employed across all sampling seasons and different intertidal areas. The four parameters (abundance, species richness, Margalef index and Shannon–Wiener diversity) from both living and total assemblages were analyzed. Surprisingly, our cluster analyses revealed that the biggest differences in community parameters were mostly due to the different tidal (low vs. 16


Y. Lei et al.

A

B

Fig. 10. Cluster analysis on Bay-Curtis similarity matrix for foraminiferal abundance of total assemblages (A) and living assemblages (B) based on monthly samplings from October 2010 to February 2012.

species richness and diversity indices in the low intertidal area were all higher than those in the high intertidal area, especially for the living foraminiferal assemblages, reflecting the seaward preference of these organisms.

high intertidal) areas, and not to the season (Figs. 10–13). However, the secondary differences resulted from seasonality. The Shannon–Wiener diversity analysis, in particular, showed that foraminiferal assemblages were clearly grouped into two different clades mainly from the two different tidal areas (Fig. 13) across all seasons. Apart from the seasonal variation in foraminifera in the intertidal zone, our result revealed, more importantly, the greatest difference in foraminiferal parameters between two tidal areas. For instance, in the low intertidal area, prominent seasonal variations in abundance, species richness and diversity were observed. Conversely, in the high intertidal area the dynamics were not distinctly seasonal. Weather influence (e.g., rainfall) and human activity impact (e.g., tourism) might be the main reasons for interference in the high intertidal area. Our Spearman's correlation analysis between individual species and environmental variables further confirmed this tendency that in the low intertidal area more species have correlations with the environmental variables than do those in the high intertidal area (Table 3). The importance of tidal impacts on benthic foraminifera has been discussed by several studies (Horton et al., 1999; Woodroffe et al., 2005; Berkeley et al., 2008; Horton and Culver, 2008) and we found some support for this. Berkeley et al. (2008) studied mangrove foraminiferal assemblages and found their absolute standing crops were different in low and high intertidal mudflats. Studies carried out in different geographic regions suggested that the distribution of foraminifera in the intertidal environment may mainly be impacted by the duration and frequency of inundation or subaerial exposure (e.g., Horton and Culver, 2008; Woodroffe et al., 2005). Our study demonstrated that the difference in the foraminiferal community parameters was primarily due to the different intertidal areas in the Yellow Sea, and so supported this point of view. Moreover, foraminiferal abundance,

5. Conclusions Community parameters (abundance, species richness, Margalef index and Shannon–Wiener diversity index) of benthic foraminifera were studied simultaneously in two intertidal (low and high) areas of the Yellow Sea. The variation in foraminifera showed a more distinct seasonality in the low intertidal area than in the high intertidal area. The dynamic of foraminiferal abundance in the low intertidal area was seasonal, with high values occurring during winter; while the other three community parameters showed variations with high values occurring in spring and autumn. In addition, the community parameters in the high intertidal area were all lower than those in the low intertidal area, reflecting a seaward preference. Cluster analyses revealed a distinct difference in foraminiferal assemblages because of tidal level (low vs. high intertidal) more than seasonality. There were also significant correlations in the low intertidal area between foraminifera and temperature or salinity, especially for salinity. For example, foraminiferal abundance, species richness and Margalef index were significantly positively correlated to salinity, while species richness was negatively correlated to temperature. Dominant species showed a similar tendency of relationships to the environmental factors. The dominant taxa of Ammonia beccarii, A. aomoriensis, A. aberdoveyensis?, A. sobrina, Quinqueloculina seminula and Murrayinella globosa from fossil cores might be used to reconstruct sea-level changes in the intertidal environment of the Yellow Sea. 17


Y. Lei et al.

A

B

Fig. 11. Cluster analysis on Bay-Curtis similarity matrix for foraminiferal species richness of total assemblages (A) and living assemblages (B) based on monthly samplings from October 2010 to February 2012.

A

B

Fig. 12. Cluster analysis on Bay-Curtis similarity matrix for foraminiferal Margalef index of total assemblages (A) and living assemblages (B) based on monthly samplings from October 2010 to February 2012.

18


Y. Lei et al.

A

B

Fig. 13. Cluster analysis on Bay-Curtis similarity matrix for foraminiferal Shannon-Wiener index of total assemblages (A) and living assemblages (B) based on monthly samplings from October 2010 to February 2012. Buzas, M.A., Hayek, L.-A.C., Jett, J.A., Reed, S.A., 2015. Pulsating Patches History and Analyses of Spatial, Seasonal, and Yearly Distribution of Living Benthic Foraminifera. Smithsonian Institution Scholarly Press, Washington D.C., pp. 1–91. Clarke, K.R., Gorley, R.N., 2006. User Manual/Tutorial. 189 PRIMER-E Ltd Plymouth. Coles, B.P.L., Funnell, B.M., 1981. Holocene palaeoenvironments of Broadland, England. Int. Assoc. Sedimentol. 5, 123–131. Debenay, J.-P., Guillou, J.-J., 2002. Ecological transitions indicated by foraminiferal assemblages in paralic environments. Estuaries 25, 1107–1120. Debenay, J.-P., Bicchi, E., Goubert, E., Armynot du Châtelet, E., 2006. Spatio-temporal distribution of benthic foraminifera in relation to estuarine dynamics (Vie estuary, Vendée, W France). Estuar. Coast. Shelf Sci. 67, 181–197. Diz, P., Francés, G., Costas, S., Souto, C., Alejo, I., 2004. Distribution of benthic foraminifera in coarse sediments, Ría de Vigo, NW Iberian margin. J. Foraminifer. Res. 34, 258–275. Erskian, M.G., Lipps, J.H., 1987. Population dynamics of the foraminiferan Glabratella ornatissima (Cushman) in Northern California. J. Foraminifer. Res. 17, 240–256. Fontanier, C., Jorissen, F.J., Licari, L., Alexandre, A., Anschutz, P., Carbonel, P., 2002. Live benthic foraminiferal faunas from the Bay of Biscay: faunal density, composition, and microhabitats. Deep-Sea Res. Part I: Oceanogr. Res. Pap. 49, 751–785. Gehrels, W.R., 1994. Determining relative sea-level change from saltmarsh foraminifera and plant zones on the coast of Maine, USA. J. Coast. Res. 10, 990–1009. Gehrels, W.R., Haslett, S.K., 2002. Intertidal foraminifera as paleoenvironmental indicators. In: Quaternary Environmental Micropalaeontology. Arnold Publishers, London, pp. 91–114 (ISBN 0-340 76198-9). Ghosh, A., Saha, S., Saraswati, P.K., Banerjee, S., Burley, S., 2009. Intertidal foraminifera in the macro-tidal estuaries of the Gulf of Cambay: Implications for interpreting sealevel change in palaeo-estuaries. Mar. Pet. Geol. 26, 1592–1599. Goineau, A., Fontanier, C., Jorissen, F.J., Lansard, B., Buscail, R., Mouret, A., Kerhervé, P., Zaragosi, S., Ernoult, E., Artéro, C., Anschutz, P., Metzger, E., Rabouille, C., 2011. Live (stained) benthic foraminifera from the Rhône prodelta (Gulf of Lion, NW Mediterranean): environmental controls on a river-dominated shelf. J. Sea Res. 65, 58–75. Gooday, A.J., Levin, L.A., Linke, P., Heeger, T., 1992. The role of benthic foraminifera in deep-sea food webs and carbon cycling. In: Rowe, G.T., Pariente, V. (Eds.), Deep-sea Food Chains and the Global Carbon Cycle. Kluwer, Dordrecht, pp. 63–91. Hayward, B.W., Hollis, C.J., 1994. Brackish foraminifera in New Zealand: a taxonomic and ecologic review. Micropaleontology 40, 185–222. Hayward, B.W., Holzmann, M., Grenfell, H.R., Pawlowski, J., Triggs, C.M., 2004. Morphological distinction of molecular types in Ammonia - towards a taxonomic revision of the world's most commonly misidentified foraminifera. Mar. Micropaleontol. 50, 237–271. Hayward, B.W., Cedhagen, T., Kaminski, M., Gross, O., 2014. World Foraminifera

Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.marmicro.2017.04.005. Acknowledgments This work received financial supports from the following projects: Strategic Priority Research Program of the Chinese Academy of Sciences XDA11030104; the National Science Foundation of China (No. 41476043, 41230959; 41430965); Continental Shelf Drilling Program of China (GZH201100202). We acknowledge Paul Brönnimann Foundation's support and the foundation president, Prof. Dr. Jan Pawlowski (Department of Genetics and Evolution, University of Geneva, Switzerland) for important supports in foraminiferal study. We gratefully acknowledge technicians Xuejiao Wang, Mengmeng Zheng and Lina Cao in sample treatments (Institute of Oceanology, Chinese Academy of Sciences). Finally, we thank Prof. Richard Jordan, the regional editor of Marine Micropaleontology and three anonymous referees for their kind help and precious comments on the manuscript. References Alongi, D.M., 1992. Benthic infauna and organism-sediment relations in a shallow, tropical coastal area: influence of outwelled mangrove detritus and physical disturbance. Mar. Ecol. Prog. Ser. 81, 229–245. Alve, E., Murray, J.W., 2001. Temporal variability in vertical distributions of live (stained) intertidal foraminifera, southern England. J. Foraminifer. Res. 31, 12–24. Berkeley, A., Perry, C.T., Smithers, S.G., Horton, B.P., Taylor, K.G., 2007. A review of the ecological and taphonomic controls on foraminiferal assemblage development in intertidal environments. Earth Sci. Rev. 83, 205–230. Berkeley, A., Perry, C.T., Smithers, S.G., Horton, B.P., 2008. The spatial and vertical distribution of living (stained) benthic foraminifera from a tropical, intertidal environment, north Queensland, Australia. Mar. Micropaleontol. 69, 240–261. Boomer, I., 1998. The relationship between meiofauna (Ostracoda, Foraminifera) and tidal levels in modern intertidal environments of North Norfolk: a tool for palaeoenvironmental reconstruction. Bull. Geol. Soc. Norfolk 46, 17–29.

19


Y. Lei et al.

Heip, C.H.R., 2000. Ecological significance of benthic foraminifera: 13C labelling experiments. Mar. Ecol. Prog. Ser. 202, 289–295. Murray, J.W., 1968. The living foraminiferida of Christchurch Harbour, England. Micropaleontology 14, 83–96. Murray, J.W., 1983. Population dynamics of benthic foraminifera: results from the Estuary, England. J. Foraminifer. Res. 13, 1–12. Murray, J.W., 1991. Ecology and Palaeoecology of Benthic Foraminifera. Longman, Harlow, pp. 1–397. Murray, J.W., 1992. Ecology and Distribution of Benthic Foraminifera: A Review. Studies in Benthic Foraminifera Benthos '90, Sendai. pp. 33–41. Murray, J.W., Alve, E., 2000. Major aspects of foraminiferal variability (standing crop and biomass) on a monthly scale in an intertidal zone. J. Foraminifer. Res. 30, 177–191. Nigam, R., 1986. Dimorphic forms of recent foraminifera: an additional tool in paleoclimatic studies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 53, 239–244. Nigam, R., 2005. Addressing environmental issues through foraminifera - case studies from the Arabian Sea. J. Palaeontol. Soc. India 50, 25–36. Nigam, R., Saraswat, R., Panchang, R., 2006. Application of foraminifers in ecotoxicology: retrospect, Perspect and Prospect. Micropaleontology Laboratory, Geological Oceanography Division, National Institute of Oceanography Dona Paula- 403 004. Environ. Int. 32, 273–283. van Oevelen, D., Soetaert, K., Middelburg, J.J., Herman, P.M.J., Moodley, L., Hamels, I., Moens, T., Heip, C.H.R., 2006. Carbon flows through a benthic food web: integrating biomass, isotope and tracer data. J. Mar. Res. 64, 453–482. Papaspyrou, S., Diz, P., García-Robledo, E., Corzo, A., Jimenez-Arias, J.-L., 2013. Benthic foraminiferal community changes and their relationship to environmental dynamics in intertidal muddy sediments (Bay of Cádiz, SW Spain). Mar. Ecol. Prog. Ser. 490, 121–135. Patterson, R.T., 1990. Intertidal benthic foraminiferal biofacies on the Fraser River Delta, British Columbia: modern distribution and paleoecological importance. Micropaleontology 36, 229–244. Pawlowski, J., 2000. Introduction to the molecular systematics of foraminifera. Micropaleontology 46, 1–12. Pawlowski, J., Holzmann, M., Tyszka, J., 2013. New supraordinal classification of foraminifera: molecules meet morphology. Mar. Micropaleontol. 100, 1–10. Phleger, F.B., 1970. Foraminiferal populations and marine marsh processes. Limnol. Oceanogr. 15, 522–534. Pujos, M., 1976. Ecologie des foraminiferes benthiques et des thecamoebiens de la Gironde du plateau continental Sud-Gascogne. (Application a la connaissaance du Quaternaire terminal de la region Ouest-Gironde). de Rijk, S., 1995. Salinity control on the distribution of salt marsh Foraminifera (Great Marshes, Massachusetts). J. Foraminifer. Res. 25, 156–166. de Rijk, S., Troelstra, S.R., 1997. Salt marsh foraminifera from the Great Marshes, Massachusetts: environmental controls. Palaeogeogr. Palaeoclimatol. Palaeoecol. 130, 81–112. Scott, D.B., Medioli, F.S., 1978. Vertical zonation of marsh foraminifera as accurate indicators of former sea levels. Nature 272, 528–531. Scott, D.B., Medioli, F.S., 1980. Living vs. total foraminiferal populations: their relative usefulness in paleoecology. J. Paleontol. 54, 814–831. Scott, D.B., Collins, E.S., Duggan, J., Asioli, A., Saito, T., Hasegawa, S., 1996. Pacific Rim marsh foraminiferal distributions: implications for sea-level studies. J. Coast. Res. 12, 850–861. Sen Gupta, B.K., 1999. Introduction to modern foraminifera. Mod. Foram. 3–6. Smith, D.A., Scott, D.B., Medioli, F.S., 1984. Marsh foraminifera in the Bay of Fundy: modern distribution and application to sea-level determinations. Marit. Sediments Atl. Geol. 20, 127–142. Wang, P.X., Zhang, J.J., Zhao, Q.H., Min, Q.B., Bian, Y.H., Zheng, L.F., Cheng, X.R., Chen, R.H., 1988. Foraminifera and Ostracoda from sediments of the East China Sea. China Ocean Presspp. 1–438. Wefer, G., 1976. Environmental effects on growth rates of benthic foraminifera (shallow water, Baltic Sea). Marit. Sed. 1, 39–50 Special Publication. Williams, H.F.L., 1989. Foraminiferal zonations on the Fraser River Delta and their application to paleoenvironmental interpretations. Palaeogeogr. Palaeoclimatol. Palaeoecol. 73, 39–50. Woodroffe, S.A., Horton, B.P., Larcombe, P., Whittaker, J.E., 2005. Intertidal mangrove foraminifera from the central Great Barrier Reef shelf, Australia: implications for sealevel reconstruction. J. Foraminifer. Res. 35, 259–270.

Database. Accessed at. http://www.marinespecies.org/foraminifera (on 2014-05-21). Horton, B.P., Culver, S.J., 2008. Modern intertidal foraminifera of the outer banks, North Carolina, U.S.A., and their applicability for sea-level studies. J. Coast. Res. 24, 1110–1125. Horton, B.P., Edwards, R.J., Lloyd, J.M., 1999. UK intertidal foraminiferal distributions: implications for sea-level studies. Mar. Micropaleontol. 36, 205–223. Jennings, A.E., Nelson, A.R., 1992. Foraminiferal assemblage zones in Oregon tidal marshes - relation to marsh floral zones and sea level. J. Foraminifer. Res. 22, 13–29. Jennings, A.E., Nelson, A.R., Scott, D.B., Aravena, J.C., 1995. Marsh foraminiferal assemblages in the Valdivia estuary, south-central Chile, relative to vascular plants and sea level. J. Coast. Res. 11, 107–123. Jian, Z., Wang, L., Kienast, M., Sarnthein, M., Kuhnt, W., Lin, H., Wang, P., 1999. Benthic foraminiferal paleoceanography of the South China Sea over the last 40,000 years. Mar. Geol. 156, 159–186. Jian, Z., Huang, B., Kuhnt, W., Lin, H.L., 2001. Late Quaternary upwelling intensity and East Asian monsoon forcing in the South China Sea. Quat. Res. 55, 363–370. Kitazato, H., Ohga, T., 1995. Seasonal changes in deep-sea benthic foraminiferal populations: results of long-term observations at Sagami Bay, Japan. In: Sakai, H., Nozaki, Y. (Eds.), Biogeochemical Processes and Ocean Flux in the Western Pacific. Terra Scientific Publishing Company, Tokyo, pp. 331–342. Le Campion, J., 1970. Contribution à l' étude des foraminifères du Bassin d'Arcachon et du proche ocean. Bulletin de l'Institut Géologique du Bassin d'Aquitaine 8, 3–98. Lei, Y., Li, T., 2015. Ammonia aomoriensis (Asano, 1951) and Ammonia beccarii (Linnaeus, 1758) (foraminifera): comparisons on their taxonomy and ecological distributions correlated to temperature, salinity and depth in the Yellow Sea and the East China Sea. Acta Micropalaeontologica Sinica 32, 1–19 (in Chinese with English abstract). Lei, Y., Li, T., 2016. Atlas of Benthic Foraminifera from China Seas the Bohai Sea and the Yellow Sea. Springer-Verlag GmbH Germany and Science Press, Beijing, pp. 1–399. Lei, Y.L., Stumm, K., Wickham, S.A., Berninger, U.-G., 2014. Distributions and biomass of benthic ciliates, foraminifera and amoeboid protists in marine, brackish, and freshwater sediments. J. Eukaryot. Microbiol. 61, 493–508. Lei, Y.L., Li, T.G., Bi, H., Cui, W.L., Song, W.P., Li, J.Y., Li, C.C., 2015. Responses of benthic foraminifera to the 2011 oil spill in the Bohai Sea, PR China. Mar. Pollut. Bull. 96, 245–260. Lei, Y., Li, T., Nigam, R., Holzmann, M., Lyu, M., 2016. Environmental significance of morphological variations in the foraminifer Ammonia aomoriensis (Asano, 1951) and its molecular identification: A study from the Yellow Sea and East China Sea, PR China. Palaeogeogr. Palaeoclimatol. Palaeoecol. http://dx.doi.org/10.1016/j.palaeo. 2016.05.010. Li, T.G., Sun, R.T., Zhang, D.Y., Liu, Z.X., Li, Q., Jiang, B., 2007. Evolution and variation of the Tsushima warm current during the late Quaternary: evidence from planktonic foraminifera, oxygen and carbon isotopes. Sci. China Ser. D Earth Sci. 50, 725–735. Li, T.G., Zhao, J.T., Sun, R.T., Chang, F.M., Sun, H.J., 2010. The variation of upper ocean structure and paleoproductivity in the Kuroshio source region during the last 200 kyr. Mar. Micropaleontol. 75, 50–61. Loeblich, A.R., Tappan, H., 1987. Foraminiferal Genera and Their Classification. Van Nostrand Reinholdpp. 1–970. Loeblich, A.R., Tappan, H., 1994. Foraminifera of the Sahul Shelf and Timor Sea. Cushman Foundation for Foraminiferal Research Special Publication 31. pp. 661. Loeblich, A.R., Tappan, H., Takayanagi, Y., Saito, T., 1992. Present status of foraminiferal classification. In: Studies in Benthic Foraminifera. Proceedings of the fourth Symposium on Benthic Foraminifera, Sendai, 1990. Tokai University Press, pp. 93–102. Lutze, G.F., 1968. Jahresgang der Foraminiferen-Fauna in der Bottsand Lagune (westliche Ostsee). Meyniana 18, 13–30. Magno, M.C., Bergamin, L., Finoia, M.G., Pierfranceschi, G., Venti, F., Romano, E., 2012. Correlation between textural characteristics of marine sediments and benthic foraminifera in highly anthropogenically-altered coastal areas. Mar. Geol. 315–318, 143–161. Manasa, M., Saraswat, R., Nigam, R., 2016. Assessing the suitability of benthic foraminiferal morpho-groups to reconstruct paleomonsoon from Bay of Bengal. J. Earth Syst. Sci. 125, 571–584. Mojtahid, M., Zubkov, M.V., Hartmann, M., Gooday, A.J., 2011. Grazing of intertidal benthic foraminifera on bacteria: assessment using pulse-chase radiotracing. J. Exp. Mar. Biol. Ecol. 399, 25–34. Moodley, L., Boschker, H.T.S., Middelburg, J.J., Pel, R., Herman, P.M.J., de Deckere, E.,

20