Foraminiferal Faunal Trends and Assemblages of the Bohai Sea, Huanghai Sea and East China Sea

BULLETIN OF MARINE SCIENCE. 47(1:): 192-212. 1990

FORAMINIFERAL FAUNAL TRENDS AND ASSEMBLAGES OF THE BOHAI SEA, HUANGHAI SEA AND EAST CHINA SEA

Shouyi Zheng

ABSTRACT Qualitative and quantitative studies of Recent foraminifera of the Bohai, Huanghai, and East China Seas gave distributional data on: faunal composition; dominant indicator species (including species occurring in high to low numbers); species diversity; faunal dominance; absolute abundance; percentage composition of agglutinated, porcelaneous and hyaline tests; planktonic/benthonic (P/B) foraminiferal ratio; and others. Correlation offaunal trends with known environmental parameters such as salinity, temperature, prevailing current and water mass systems, substrate, CaCO, content of sediment, and more allowed establishment of foraminiferal assemblages useful for ecological and paleoecological interpretations. Based on marked changes in frequency composition among dominant benthic species, six benthonic assemblages were recognized in the Bohai Sea, three in the northern Huanghai Sea, five in the southern Huanghai Sea, and nine in the East China Sea. In addition, four planktonic assemblages characterized the East China Sea and southern Huanghai Sea.

The small size, great abundance and wide distribution of their preservable tests in Recent and fossil sediments, together with their usefulness as environmental indicators, has resulted in more comprehensive study of foraminifera than most other marine protozoa. Their sensitivity to environmental changes is reflected in various specific and non-specific distributional trends. The cumulative occurrence of their preservable tests on the sea floor mirrors not only small-scale temporal and spatial features, but also long-term average environmental and taphonomic processes.

PHYSIOGRAPHY AND HYDROGRAPHY OF THE AREA STUDIED

The three seas under study for their foraminiferal trends cover a range of 15 degrees of latitude (Fig. 1). Each sea has its distinctive set of physical and hydrological characteristics which control the distribution of the foraminifera. The East China Sea, averaging 370 m in depth, ranges from a few meters to 2,719 m. It is largely influenced by the warm, saline Kuroshio Current and its branches, the Taiwan Warm Current, the Tsushima Warm Current, and the Huanghai Warm Current (Fig. I). It has an average surface water temperature of 28°C in summer and II-21°C in winter. The average surface salinity is 300/00at the Changjiang River mouth and 34.50/00in the main Kuroshio area in the southeastern part of the sea. The southern Huanghai Sea ranges in depth from a few meters to 103 m, averaging 46 m. The average surface and bottom temperatures are 25-27°C in summer, and 5-lQoC in winter, with salinities of 31-340/00.It is influenced by the cold Huanghai Sea Coastal Current and the Huanghai Sea Cold Water Mass. The northern Huanghai Sea ranges in depth from a few meters to 70 m. Average surface to bottom winter temperatures are 0-5°C; summer temperatures are 25-27°C. Salinity averages 31- 320/00. The Bohai Sea ranges in depth from a few meters to 70 m, averaging 18 m. Three bays surround its central basin. Its yearly average salinity is 300/00.The average surface temperature is 22-28OC, largely influenced by its surrounding continental climate. According to Backus' (1986) map of world biogeographic regions, the East China Sea falls into the northern subtropical region, the southern Huanghai Sea into the northern subtropical to northern temperate regions, and the northern Huanghai Sea and Bohai Sea into the northern temperate biogeographic region. Previous works wholly or partly touching on the foraminifera of these seas include those of Jacot (1952); Bezrukov et aI. (1958); Polski (1959); Waller and Polski (1959); Cheng and Cheng (1960, 1962, 1963); Zheng, Zheng and Fu (1979); Stschedrina and Lukina (1984); Wang et a1.(1984); Zheng (1988).

192 ZHENG: FORAMINIFERAL TRENDS OF CHINA SEAS 193

Figure 1. Distribution of current systems (after Guan, 1983), Huanghai Sea Cold Water Mass (after He et aI., 1959), Changjiang Diluted Water (after Le, 1980).

MATERIALS AND METHODS

Study materials were foraminiferal tests from more than 500 surface sediment grab samples collected over a 30-year period from longitudes 118°00-120"00'E and latitudes 26°28'-41°00'N. Collection depths ranged from a few meters to over 2,000 m (Fig. 2). The samples represent great environmental variability; they were collected from semi-enclosed bays, river mouths, vast expanses of continental shelf, and bathyal depths. A unit weight of 50 g of dried sediment was used for quantitative analysis. The samples were washed on a 150 Ilm-opening screen. Foraminifera were floated with carbon tetrachloride (sp. gr. 1.59). Floated concentrates were weighed by torsion balance to obtain total weights per 50 g of sediment. Specimen 194 BULLIETIN OF MARINE SCIENCE, VOL. 47, NO. I, 1990

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ANALYSIS OF DISTRIBUTION Parameters Considered for Benthonic Foraminifera Taxonomic Composition. - A sudden appearance, disappearance or a radical change in abundance of an abundant organism along a transect is usually indicative of a change in environmental conditions (presence of a boundary, Backus, 1986). In this study, results show that ranking changes among the 10 most abundant species define broad geographic differences in environmental regimes. While different regions have dominant species common to each other, each region has its own characteristic taxonomic composition (Tables 1, 2). A north to south transect at longitude 123°30'E, extending from 39°23'N in the northern Huanghai Sea to 26°30' in the East China Sea (Fig. 2), clearly shows increasing change in taxonomic composition with latitude (Table 2). Changes in taxonomic composition across physically generated environmental gradients are clearly evident in a southern transect (Fig. 3) at latitude 27°N, covering longitudes 121-127°E, cutting across the shelf to a depth of 1,300 m. The most marked change occurs at Stn. £196 in the bathyal region where the five most abundant species (Cribrostomoides crassimargo (Norman), Cyclammina pusilla Brady, Tro- chammina globigeriniformis (Parker and Jones), Cribrostomoides subglobosa (G. O. Sars), and Globocassidulina subglobosa (Brady)) differ entirely from those of the preceding station El94 on the slope (Heterolepa cushmani (Ujiie and Kusu- kawa), Spirorutilis fistulosa (Brady), Cribrobigenerina textularioidea (Goes), Len- ticulina calcar (Linne), and Fontbotia wuellerstorfi (Schwager)). Dominant and Indicator Species. - Distributional patterns of many benthonic foraminifera are controlled by and/or correlated positively with the variables that characterize different water masses and which may fluctuate in space and time (Van Morkhoven et aI., 1986). Species, however, have upper depth limits con- strained by biology that may make them useful as depth zone indicators. For example, Rotalinoides gaimardii (d'Orbigny) is the most abundant species in almost all middle to outer shelf samples in the East China Sea. Its relative abundance decreases northward, and in the shallower water of the northwestern Huang- hai Sea and the Bohai Sea it is not within the five most dominant species (Table 3). Thus it appears characteristic of middle to outer shelf conditions (though other variables associated with more northerly and inshore locations may playa role). Arenoparrella asiatica (Polski), on the other hand, is very abundant in shallow, nearshore areas (<50 m depth) throughout the area of investigation and may rank 196 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.1, 1990

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Figure 3. Variation in foraminiferal faunal trends along Transect IIIat latitude 27·N, longitude 121· to 127·E, East China Sea. S-number of species, V -faunal variability, D-faunal dominance of the five most abundant species, H(S)-Shannon-Wiener diversity index, E-Buzas-Gibson equitability index, N-number of tests· 50 g-I dried sediment sample. I Rotalinoides gaimardil, 2 Elphidium advenum, 3 Hanzawaia compressa 4 Arenoparrella asiatica, 5 Ammonia annectens, 6 Bigenerina nodosaria, 7 Heteralepa cushmani, 8 Hanzawaia nipponica, 9 Siphonapertaprominentis, 10Heterolepa subpraecincta. 11 Discorbinella bertheloti, 12 Spiroloculina communis, 13 Textularia foliacea, 14 Quinqueloculina ungeriana, 15 Spirorutilis fistulosa, 16 Quinqueloculina akneriana. 17 Textularia pseudogramen, 18 Caribeanel/a sp., 19 Planorbulinella larvata, 20 Cribrobigenerina textularioidea, 21 Lenticulina calcar, 22 Fontbotia wuellerstorfi, 23 Cribrostomoides crassimargo, 24 Cyclammina pusilla, 25 Trochammina globigerinijormis. 26 Cribrostomoides subglobosa, 27 Globocassidulina subglobosa. ZHENG: FORAMINIFERAL TRENDS OF CHINA SEAS 199 among the five most abundant species. At depths greater than 50 m, it is rare to absent. Some numerically rare species occur only within a particular environment; this gives them indicator significance. They may also (numerically) dominate the faunas or assemblages in which they occur. For example, Pseudoeponides anderseni Warren, although few in number, occurs in most samples from Hangzhou Bay; the Bay contains few foraminfera, probably due to hyposalinity. Cuneata arctica (Brady), Reophax micaceous Earland, Spiroplectammina hiformis (Parker and Jones), Textularia torquata Parker, and T. antarctica (Wiesner) are known for their restriction to cold waters elsewhere; here they are found only at 40-50 m depths in the Huanghai Sea Cold Water Mass area (northern Huanghai Sea). The limited distribution of other numerically rare species such as Cornuloculina in- constans (Brady), Bathysiphonfiliformis (M. Sars), and Glomospira charoides (Jones and Parker), at bathyal depths in the Okinawa Trough, establishes them as ex- cellent deep-water indicators (Zheng and Fu, 1988). Species Diversity. -Differences in species diversity (numbers of species) among samples within a single biogeographic area mark differences in environment. Such differences can be seen clearly in a southern transect in the East China Sea, extending from inshore to bathyal depths (Fig. 3). In general, species diversity is lowest in nearshore coastal zones and in marginal marine environments. It increases offshore toward neritic depths where it reaches its maximum. Still at a maximum or beginning to show a decrease in the upper bathyal region, species diversity finally decreases at deeper bathyal depths. Deviations from the normal pattern have environmental implications. For example, in the southern Huanghai Sea, species diversity is highest in the shoreward western half ofthe sea but gradually decreases northward and offshore. This correlates with the presence ofthe Huanghai Sea Cold Water Mass on the bottom in this region. This cold water mass appears favorable for the existence of only a few species. Figure 3 shows abnormally high H(S) values at station E 189(longitude 122°30'E) compared to stations E187 and E190, before and after it. This station is in the area of the western front of the Taiwan Warm Current (Weng and Wang, 1984), which may affect the fauna. The central part and strait area of the Bohai Sea, influenced by intruding warmer waters carried by a weakened branch of the Huanghai Warm Current, have much higher diversity values than the other parts of the sea. In the East China Sea, in general, values for S, V, and H(S) all show an increasing trend across the outer shelf region up to the shelf edge. Beyond it S and V values show a rapid decrease while H(S) values still show a steady increase and finally reach a maximum at bathyal depths (Fig. 3). This trend accords with the general rule that deep water environments are more stable than shallow environments and that species equitability (evenness of distribution) among deep sea foraminifera is greater than in shallow depths (Gibson and Buzas, 1973; Boltovskoy and Wright, 1976; Douglas, 1979). Differences in diversity trends of the three seas seem to be related to habitat heterogeneity. The East China Sea has the greatest environmental variability and the highest species diversity (Table 2). Habitat variability may account for the high diversity values in the Bohai Sea, as suggested by its three bay assemblages with quite different species compositions (Table 2; Fig. 4). Faunal Dominance. -In general, faunal dominance is inversely related to taxonomic diversity (Tipsword et ai., 1966; Boucot, 1981)-that is, the greater the 200 BULLETIN OF MARINE SCIENCE, VOL. 47, NO. I, 1990

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...." ,. - -28' ." - - - - - £ - V b ...... --E- V rr 13-3J-29- ~9-39-13- 33-38 I 23-5 zoa c 118 120' 122' 124' 120 12R" 130"E Figure 4. Areal distribution of benthonic foraminiferal assemblages of the Bohai Sea, Huanghai Sea and East China Sea (faunal characteristics summarized in Table 3). Solid line- boundary of assemblage. Dashed line-boundary of subassemblage. Arabic numbers are the equivalents of the five most abundant species. Dotted lines- Rass' (1986) climatic biogeographic boundaries crossing the East China Sea based on the inset map. The region above the first line falls into the southern boreal region; the region below the second line, the equatorial region; the region between the two lines, the tropical region. 202 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.1, 1990 percent of the fauna made up by one to a few species, generally the fewer the total number of species present. Usually only a few species are adapted to nearshore and other areas where environmental conditions vary greatly, or depart too much from normal marine. In addition, when taxonomic diversity is low, faunal dominance by one to a few species often is great, with these species making up high percentages of the fauna (Boucot, 1981). Such great faunal dominance generally is at a maximum in intertidal zones (or other high-stress areas) and decreases offshore to a minimum off the edge of the continental shelf(Tipsword et aI., 1966). In this study, the cumulative percentage of the five most abundant species (Dms) in a sample was used as an index of faunal dominance. Deviations from the normal trend have environmental implications. For example, stations SH38- SH46 along Transect II (latitude 35°N, longitudes 119°30'E in the Haizhou Bay to 124°15'E) showed seaward D values of71%, 70%, 71%, 75%, 73%, 88%, 94%, 99%, and 95%, respectively (Fig. 2). Stations SH43-SH46 have Ammonia ketienziensis angulata Kuwano as the most abundant or highest ranked species. This species' main distribution area is characterized by mixed water masses (Huanghai Sea Cold Water Mass and the Huanghai Mixed Water reported by Mao et aI., 1965; Ren et aI., 1965). The low salinity Changjiang Diluted Water also influences this area; here the 310/00isopleth may extend northeast to Jizhou Island (Chejudo 1.), almost covering the northwestern part of the East China Sea (Guan, 1983). Faunal dominance values (Dms) within the same depth range vary among regions. For example, in the 11-20 m depth range, the Bohai Sea registers an average Dms value of75%, the northern Huanghai Sea, 84%, the southern Huang- hai Sea, 82%, and the East China Sea, 90%. However, in the 50-60 m depth range, all four regions have Dms values ranging from 82 to 85%. At this depth range, the average H(S) values for the four regions are consistently low. Beyond this depth range, the Dms values drop to <80% and H(S) values increase to >2. This trend indicates a general change in both the physiographic and hydrological environments, from below normal inner shelf conditions to normal marine middle shelf and outer shelf conditions. Absolute Abundance. - Within their areas of distribution, animals occur in varying densities in response to environmental gradients. Entire faunas also show quantitative abundance variation in their horizontal (areal) as well as vertical (depth) distributions. In this study absolute abundance generally increases with increased distance from shore (Fig. 5). Low densities of < 10 tests' 50 g-l sediment off the Changjiang River mouth relate to hyposalinity and dilution by rapid sedimentation. Seaward, density values increase rapidly to a maximum in the shelfregion, and then decrease at bathyal depths. Table 2 shows that the Bohai Sea, which departs most from normal marine conditions, has the lowest average benthic foraminferal density oftlhe three seas. The East China Sea has the highest average density, with more than half the total number of stations registering 103 to 104 tests· 50 g-l sediment. It also has the greatest patchiness of abundance distribution, which may result from its having the greatest environmental heterogeneity (Fig. 5). The small-sized foraminifera, with their diversity of species, here seem to respond well to the mosaic nature of the environment. (It should be remembered that the present study was of foraminiferal tests from bottom sediments; live vs. dead specimens were not differentiated and taphonomic processes were not in- vestigated.) Test Composition. - The relative proportion of the three major groups of benthic foraminifera (agglutinated, porcelaneous, and hyaline) has been used to interpret ZHENG: FORAMINIFERAL TRENDS OF CHINA SEAS 203

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120' 124· 12K" E Figure 5. Horizontal quantitative distribution of benthonic foraminifera in the Bohai Sea, Huanghai Sea and East China Sea. 204 BULLETIN OF MARINE SCIENCE, YOLo 47, NO.1, 1990 water depth, water temperature, and salinity and climate (Douglas, 1979). Agglu- tinated tests often increase and constitute the largest percentage of the fauna in marshes, near the effluence of rivers, and at bathyal depths (lysocline and CaC03 compensation depths). At the Hangzhou Bay mouth in the East China Sea and in the nearshore areas where the Yalu River empties into the northern Huanghai Sea, frequences of > 40% agglutinated tests were recorded. A few stations in the Okinawa Trough have values as high as 50%. Calcareous imperforate porcelaneous foraminifera are usually most abundant and diverse in continental shelf or shallow waters of low and middle latitudes and rare to absent in lower bathyal and abyssal environments. They live where CaC03 is sufficiently available for the tests. In the East China Sea, off the mouths of Hangzhou Bay and the Changjiang River, porcelaneous forms make up as much as 30- 50% ofthe benthic foraminiferal fauna. With depth increase toward the middle shelf, abundance decreases to < 10%, but increases again to 10-15% on the outer shelf. Porcelaneous tests are at a minimum in the slope and trough regions (Zheng and Fu, 1988). In the Bohai Sea, the Bohai and Laizhou Bay mouths are bounded by the 20-30% porcelaneous foraminiferal isopleth. The calcareous perforate or hyaline foraminiferal tests are usually the most abundant shell type above mid bathyal depths, mainly making up > 50% of the benthic foraminifera fauna and increasing with depth through the upper bathyal zone. This trend is most evident in the southeastern Huanghai Sea where they make up > 90%. In the East China Sea, these hyaline forms are most abundant on the slope where they make up 80-90%, decreasing to < 50% lower in the bathyal zone. They reach minimum values of <30% in the coastal waters of Zhejiang Province.

Benthonic Foraminiferal Assemblages Benthonic foraminifera respond to environmental changes; this is reflected in their various faunal trends. Marked taxonomic change of the five most dominant species from one area to another constitutes the main basis for delineating (en- vironmentally related assemblages). Other faunal trends such as distribution of absolute abundance, diversity values, dominance values, proportion of the three major shell types, and planktonic/benthonic ratios, were also considered. Cor- relation of (known) environmental conditions with occurrences of particular assemblages gives the assemblages environmental significance. Based on the above criteria, 23 thanatotopic benthonic assemblages were delinated. There are six for the Bohai Sea (B-1 to B-YI), three for the northern Huanghai Sea (NH-l to NH-III), five for the southern Huanghai Sea (SH-I to SH- V), and nine for the East China Sea (E-I to E-IX) (Fig. 4). Each shows characteristic faunal trends as summarized in Table 3. Highlights of these trends are discussed below. Bohai Sea Assemblages. - Fifteen species, variously ranked and distributed, constitute all the dominants in the six assemblages delinated (five for each assemblage). The three Bay assemblages (Liaodong (B-1), Bohai (B-II), and Laizhou Bays (B-III)) appear distinct from each other. Eleven species make up the three sets of dominants. Ammonia annectens (Parker and Jones) ranks second in As- semblage B-1 and third in B-III. The others of the first to third ranking bay assemblage species differ. Textulariafoliacea Heron-Allen and Earland as first ranking species character- izes assemblage B-VI from the central Bohai Sea. Its presence there correlates ZHENG: FORAMINIFERAL TRENDS OF CHINA SEAS 205 well with the presence of warm water (from weak extensions of the Huanghai Warm Current). Northern Huanghai Sea Assemblages. - Three assemblages were delineated. Twelve species comprise the three sets of (five each) dominants. Assemblage NH-I, from off the northern Shandong Peninsula, is characterized by having Textulariafoli- acea as first ranking species. This assemblage is from the warm water region and has the highest species diversity. Assemblage NH-II from the northernmost Huanghai Sea is characaterized by a dominance of agglutinated species, with the first three species-Proteonella difflugiformis (Brady), Reophax bilocularis Flint, and R. scorpiurus Montfort making up 73%. It also shows a general paucity of foraminifera. The assemblage's location correlates with low sediment CaC03 and hyposalinity. Assemblage NH-III is similar to Assemblage SH-IV of the mid- southern Huanghai Sea in havingAmmonia ketienziensis angulata and H anzawaia nipponica as co-dominants. Southern Huanghai Sea Assemblages. -Assemblages SH-IV and SH-V both fea- ture Ammonia ketienziensis angulata as the highest ranked species. Assemblages SH-I and SH-II share having Ammonia annectens in first or second rank, and SH-I and SH-III share having Textulariafoliacea in first or second rank. Beyond that, considerable difference exists among the five dominant species at each of the five stations. East China Sea Assemblages. -Nine assemblages with four subassemblages were delineated. Thirty different species constitute the dominants. Assemblage E-I from the Changjiang River mouth and Hangzhou Bay is distinguished only by having Rotalinoides gaimardii (d'Orbigny), the number one dominant species in middle to outer shelf samples, as its fifth ranking species. Assemblage E-III represents a mixture of Huanghai and East China Sea species. Using species diversity, it is subdivided into two subassemblages. Subassemblage E-IIIa differs from E-IIIb by a lower species diversity (S = 21, V = 7, H(S) = 1.3 versus S = 33, V = 16, H(S) = 2.2) and higher faunal dominance (Dms = 92% verSUSDms = 75%), and shows greater similarity to the Huanghai Sea assemblages. The southern boundary ofE-IIIb's occurrence roughly coincides with the southernmost extent ofHuanghai Mixed Water influence. Assemblage E-IV, located in the Huanghai Sea Warm Current area, is mixed and consists of species characteristic of the Huanghai and East China Seas. It differs from all other assemblages in having Gyroidinoides nipponica (Ishizaki) and Bolivina robusta Brady as dominant species. These two species were reported by Kim and Han (1972) from the southeastern coast of Korea. Assemblage E-V, from the middle shelf region south of 30oN, is divided into two subassemblages based on different fourth and fifth most abundant (ranking) species. Subassemblage E-Va is characterized by higher total faunal dominance values. Subassemblage E-Vb is characterized by much higher species diversity, lower total abundance, much lower faunal dominance, and much higher P/B ratios. These trends indicate greater proximity to the open ocean. Assemblage E-VI contains dominant Quinqueloculina akneriana d'Orbigny and Elphidium advenum Cushman, characteristic of shallow water assemblages. The locations of Assemblages E-VI and VII (also having Q. akneriana as dominant species) mark an outer shelf area where Niino and Emery (1961) reported relict sediments. Assemblage E-VIII, from the slope north of 30oN, has Bulimina aculeata d'Or- bigny and Hyalinea balthica (Schroeter) as first and second most abundant species. 206 BULU,TIN OF MARINE SCIENCE, VOL. 47, NO. I, 1990

It is characterized by having a species composition entirely different from the outer shelf edge E-VI and E-VII assemblages and by having high PIB ratios. The other species are typical of deeper waters. Assemblage E-IX from the Okinawa Trough is characterized by Uvigerina di- rupta Todd and Fontbotia wuellerstorfi (Schwager) as first and second most abundant species. The other three dominant species are typical of deep-water. This assemblage reaches a study maximum PIB ratio of 125.6.

Planktonic Foraminifera Distributional patterns ofliving planktonic foraminifera show that most species are very sensitive to water-mass properties such as temperature, salinity and oxygen content, hence their usefulness as oceanographic and palaeoceanographic indicators. They are usually studied in relation to the distribution of large-scale oceanic circulation. In a n~latively small area such as the East China and southern Huanghai Seas, which are marginal parts of the Pacific Ocean, the study of the distributional trends of this group is also significant. This is because the environmental tolerances of different species can be ascertained, thus establishing their roles as indicator species or assemblages. Thirty species of planktonic foraminifera were found in the >0.5 mm fraction of the samples from the East China Sea. Neogloboquadrina eggeri (Rhumbler), Pulleniatina obliquiloculata (Parker and Jones), Globigerinoides ruber (d'Orbigny), G. sacculifer (Brady), and Globigerina bulloides d'Orbigny were the five most abundant species and made up 84% of the total abundance. Only five species were found in the southern Huanghai Sea. In order of decreasing relative abundance, these are Globigerina bulloides, Neogloboquadrina eggeri, Globigerinoides ruber, G. sacculifer, and Globorotalia inflata (d'Orbigny). No planktonic foraminfera were found in the northern Huanghai Sea nor Bohai Sea. Species diversity decrease correlates with increased latitude, shallowing and proximity to shore and with decreased surface temperatures. Diversity is at a maximum (> 20 species) south of latitude 300N in the Kuroshio Current region (Fig. 6). Figure 7 shows the quantitative distribution of planktonic foraminifera in the study area. Consistent with the high species diversity there, specimens are most abundant in the Kuroshio Current region where surface temperatures and salinities are high. The> 5,000 tests· 50 g-t isopleth more or less corresponds to the location and flow direction of the Kuroshio Current, the Taiwan Warm Current and the Huanghai Warm Current. North of approximately 32°N, planktonic foraminifera are distributed northwesterly toward the central southern Huanghai Sea. They occur in gradually decreasing densities where the Huanghai Sea Warm Current prevails. Between approximately latitudes 33°-35°N, their scattered occurrences suggest that the Huanghai Sea Warm Current has experienced a rapid lowering of temperature (Ren et aI., 1965) The northward limit of planktonic foraminiferal distribution corresponds roughly to the southern boundary of the Huanghai Sea Cold Water Mass. Perhaps shallowing, continental influences (possibly sediment), and geographic seaway restriction have created an environment unfavorable to planktonic foraminifera. Fairly dense concentrations of planktonic foraminifera off the Zhejiang coast between longitudes 122-1 24°E correlate with the presence of the Taiwan Warm Current as delineated by Weng and Wang (1984). The peak of the 100 tests· 50 g-l sediment isopleth in this region corresponds closely to the northern front of the Taiwan Warm Current, which may reach 31°N (Weng and Wang, 1984). On the (shallow) inner shelf where a relatively cold coastal current prevails, and also ZHENG: FORAMINIFERAL TRENDS OF CHINA SEAS 207

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0 26 0 0 118 1;0 1~20 1240 1260 1280 1300E Figure 6. Planktonic foraminifera assemblages of the East China Sea and southern Huanghai Sea. R-G/obigerinoides ruber; E-Neog/oboquadrina eggeri; S-G/obigerinoides saccu/ifer; C-Globigeri- noides cong/obatus; B-G/obigerina bu//oides; O-Pu//eniatina obliqui/ocu/ata; A-Tinophode//a am- bitacrena; I-Globorotalia inj/ata. First number in parentheses is the average total number of species; second number is the average total number of tests per fifty grams of dried sediment. 208 BULLETIN OF MARINE SCIENCE, VOL. 47, NO. I, 1990 in runoff areas of Hangzhou Bay and the Changjiang River, planktonic foraminifera occur in very low numbers. In the region of Huanghai Mixed Water influence, its flow direction and extent of influence are indicated by two distinct bulges of the 5,000 tests' 50 g-I isopleth (Fig. 7). The most pronounced bulge extends southerly between 124 and 125°E, at approximately latitude 28°N; this corresponds to the southern extent of influence of the summer 20 m Huanghai Mixed Layer (Mao et aI., 1965). The other bulge extends southeasterly at longitude 127°30'E, just north oflatitude 300N. At roughly longitudes 122-l23°E, latitude 26°30'N, the pattern of density isopleths corresponds more or less to the flow direction of surface currents northeast of Taiwan (Weng and Wang, 1984). The relative proportion of planktonic to benthonic foraminifera (P/B ratio) is a useful index of distance from shore. As the water column deepens away from the coast, usually planktonic foraminifera progressively increase relative to benthonic foraminifera. P/B ratios are highest in the southeastern outer portion of the East China Sea, strongly influenced by the Kuroshio, and gradually decrease shoreward and northerly. On the whole, a basic similarity exists in the study area in the distribution patterns of planktonic sp~:cies. The relative abundance distributions show, however, that some, such as Globorotalia menardii (d'Orbigny) and Sphaeroidinella dehiscens (Parker and Jones), are relatively stenotopic. They are more restricted to open-ocean areas where surface waters are high in salinity and temperature. Other species, such as Globigerinoides ruber and Globigerina bulloides, are relatively eurytopic. They are more widely distributed, and may occur where temperatures are lower. Globigerina bulloides, often considered a cool-water species, may occur in areas of upwelling cold water that are surrounded by warmer water. Based on marked changes in relative abundance and dominance rankings of the five most abundant planktonic species, they can be separated into four assemblages with characteristic distributional trends of species number and total abundance (Fig. 6). Subassemblages show gradual changes in dominance ranking of particular species with environmental change.

ZOOGEOGRAPHIC CONSIDERA nONS Analysis of foraminiferal faunal trends at fine scales shows distributional variability. These trends are useful for ecological, paleoecological, and also for zoogeographic studies. The Bohai Sea, Huanghai Sea, and East China Sea are marginal parts of the Pacific Ocean and thus are often not included in large-scale biogeographic studies. Boitovskoy and Wright (1976) provided a map of world biogeographic provinces based on foraminifera. They designated the regions discussed herein as the Sinian Province and distinguished temperate water faunas north of approximately 300N (including the Huanghai and Bohai Seas) from warm water faunas to the south. Rass (1986) extended two biogeographic boundaries across the East China Sea in his map of the climatic biogeographic regions in the world oceans. One line extends obliquely from :=:::latitude32°30'N, longitude 1300E to the Zhejiang coast at :=:::latitude 29°30'N, longitude l22°E. Another line extends obliquely from :=:::latitude 30045'N, longitude l300E to the Fujian coast at :=:::latitude26°45'N, longitude l200E. The southeastern part of the East China Sea would thus be included in his equatorial region and the northern part in his northern boreal region. The narrow zone between these two lines was designated the tropical region (Fig. 4, inset map). The overall distributional trends of both the planktonic and benthonic foraminifera in the present study show that at approximately latitude 300N, marked ZHENG: FORAMINIFERAL TRENDS OF CHINA SEAS 209

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26· 0 1180 1200 122 12.1° 126· 1280 [300E Figure 7. The relation between the quantitative distribution of planktonic foraminifera and the distribution of prevailing water and current systems in the East China Sea and Huanghai Sea. 1. Number of tests· 50 g-I dried sediment; 2. August mean bottom temperature (showing the area of the Huanghai Sea Cold Water Mass) (He et aI., 1959); 3. Boundary of water systems (surface layer) in winter; 4. Warm current; 5. Huanghai Mixed Water; 6. Coastal current (3,4,5,6, Ren et ai., 1965). 210 BULLETIN OF MARINE SCIENCE, VOL. 47, NO.1, 1990 changes take place. Table 2 shows that the four most abundant benthonic foraminferal species of stations E46 and E65 at 31°00'N and 30030'N, respectively, are entirely different from station E28 at latitude 31°25'N. The East China Sea benthonic fauna is not a characteristically tropical one, however, when compared with the foraminifera of the South China Sea, including those of the Xisha and Zhongsha islands (Cheng and Zheng, 1978; Zheng, 1979; Zheng, 1980). Many typical tropical species never reach this region. Therefore, it is reasonable to consider the southern East China Sea- south of latitude 300N -as part of the northern subtropical biogeographic region. Then the northern East China Sea (north of 300N), the Huanghai Sea, and the Bohai Sea belong to the northern temperate biogeographic region. The East China Sea and southern Huanghai Sea planktonic foraminifera as a whole belong to the warm-water "central fauna" (Bradshaw, 1959; Cheng and Cheng, 1963). The fauna's warm water nature is best represented by Assemblage I (Fig. 6) which has a maximum species diversity and total abundance. The shoreward boundary of this assemblage's area is bounded by the 23°C average annual surface isotherm and the > 340/00isohaline (Cheng and Cheng, 1963). The assemblage shows a much stronger tropical character than do the other three. Yet, there are no representatives here of some species limited to the very tropical equatorial west central fauna of Bradshaw (1959) such as Globoquadrina con- glomerata (Schwager), Hastigerinopsis digitiformans Saito and Thompson and Globorotaloides hexagona (Natland). These taxa are not common, however, and their distributions may not be clear. Therefore the East China Sea planktonic foraminiferal fauna as a whole mayor may not be considered strictly tropical in this part of the world.

CONCLUSIONS Benthonic and planktonic foraminiferal assemblages from a large area off the coast of the People's Republic of China were delineated in this study of thousands offoraminifera. The differing assemblages were based on species composition and dominance ranking of the five most abundant species. The marked changes in the faunas and their trends are consistent with and indicate significant environmental changes. Six, three, five and nine benthonic foraminiferal assemblages were recognized from the Bohai Sea, northern Huanghai Sea, southern Huanghai Sea, and East China Sea, respectively. Four planktonic foraminiferal assemblages also were recognized in the East China Sea and southern Huanghai Sea. Their distributions are indicative of different biogeographic regions. Based on overall species composition of their foraminiferal faunas, the southern East China Sea, roughly south of 30oN, belongs to the subtropical biogeographic region; the northern half ofthe East China Sea, the Huanghai Sea and the Bohai Sea belong to the northern temperate biogeographic regions.

ACKNOWLEDGMENTS

I am grateful to the following persons and groups for their assistance in this lengthy project. Sediment samples were provided by the Invertebrate Zoology and Marine Geological Departments of the Institute of Oceanology, Academia Sinica. Z. Fu has assisted with the figures. Helpful reviews of the manuscript were provided by an anonymous reviewer and Dr. Roberta K. Smith. Dr. Smith also kindly assisted me in manuscript revision.

LITERATURE CITED

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Bezrukov, P. L. et al. 1958. On sediments and benthonic foraminifera in the northern East China Sea. Oceanologia et Limnologia Sinica 1(3): 269-315. (In Chinese, with Russian abstract) Boltovskoy, E. and R. Wright. 1976. Recent Foraminifera. W. Junk b.v. Publishers, The Hague, 515 pp. Boucot, A. J. 1981. Principles of benthic marine palaeoecology. Academic Press, Inc., New York. 463 pp. Bradshaw, J. S. 1959. Ecology of living planktonic foraminifera in the north and equatorial Pacific Ocean. Contr. Cushman Found. Foram. Res. (10) (196): 25-64, pis. 6-8, figs. 1-43. Buzas, M. A. and T. Gibson. 1969. Species diversity and benthonic foraminifera in the western North Atlantic. Science 163: 72-75. Cheng, T. and S. Cheng. 1960. The planktonic foraminifera of the Yellow Sea and the East China Sea. Oceanologia et Limnologia Sinica 3(3): 125-156, II pis. --- and ---. 1962. On the ecology of the planktonic foraminifera of the Yellow Sea and East China Sea. Ibid. 4(1-2): 60-85, I pI. --- and ---. 1963. An attempt at a preliminary delineation of the geographic regions of planktonic foraminifera of the Yellow Sea, the East China Sea and adjacent waters. Ibid. 5(3): 207-214. --- and S. Zheng. 1978. The Recent foraminifera of the Xisha Islands, Guangdong Province, China. I. Studia Marina Sinica, no. 12: 149-266,33 pis. Douglas, R. C. 1979. Benthic foraminiferal ecology and paleoecology: a review of concepts and methods. SEPM Short Course No.6, Houston, 21-53. Gibson, T. and M. A. Buzas. 1973. Species diversity: patterns in modern and Miocene foraminifera of the eastern margin of N. America. Geol. Soc. Am. Bull. 84: 217-238. Guan, B. 1983. A sketch of the current structures and eddy characteristic in the East China Sea. Proceedings ofInternational Symposium on Sedimentation on the Continental Shelf with Special Reference to the East China Sea. China Ocean Press, Beijing, 52-73. He, C., Y. Wang, Z. Lei and S. Xu. 1959. A preliminary study ofthe formation of Yellow Sea Cold Water Mass and its properties. Oceanologia et Limnologica Sinica 2(1): 1-15. (In Chinese with English Abstract) Jacot, A. P. 1952. Shantung Foraminifera. Jour. of the North China Branch of the Royal Asiatic Society 56: 76-79. Kim, B. K. and J. H. Han. 1972. A foraminiferal study of the bottom sediments of the southeastern coast of Korea. United Nations ECAFE, CCOP Tech. Bull. 6: 13-28, pis. II-I to 11-4. Le, K. 1980. A preliminary study on the salinity distribution and the current structure of the Changjiang Diluted Water. in "Proceedings of the Symposium of Hydro-Meteorological Society of China, Nov. 1980 Amoy." Mao, H., R. Ren and G. Sun. 1965. Preliminary analysis of summer hydrological characteristics of the southern Huanghai Sea and northern East China Sea (28°-37°N) and sea water type (water systems). Studia Marina Sinica 01: 27-77. (In Chinese) Niino, H. and K. O. Emery. 1961. Sediments of shallow portions of East China Sea and South China Sea. Geol. Soc. Am. Bull. 72(5): 731-762. Polski, W. 1959. Foraminiferal biofacies off the North Asiatic coast Jour. Pal. 33(4): 569-587, 1 pI. Rass, T. S. 1986. Vicariance ichthyogeography of the Atlantic Ocean pelagial. Pages 237-241 in A. C. Pierrot-Butts et aI., eds. Pelagic biogeography. Unesco Tech. Pap. Mar. Sci. Unesco. Ren, R., G. Sun and H. Mao. 1965. A preliminary analysis of the winter hydrological characteristics and sea water types (water systems) of the southern Huanghai Sea and northern East China Sea (28°-37°N). Studia Marina Sinica 01: 78-12. (In Chinese) Stschedrina, Z. G. and T. G. Lukina. 1984. Foraminifera of Pacific Shelf in Southeastern Asia. USSR Acad. Sci. Zool. Inst. Leningrad, 141 pp., 31 pis. (in Russian) Tipsword, H. L., F. M. Setzer and F. L. Smith. 1966. Interpretation of depositional environment in Gulf Coast petroleum from paleoecology and related stratigraphy. Trans. Gulf Coast Ass. Geol. Soc. 16: 119-130. Van Morkhoven, F. P. C. M., W. A. Berggren and A. S. Edwards. 1986. Cenozoic cosmopolitan deep-water benthic foraminifera. Bull. Centres Rech. Explor.-Prod. Elf-Aquitaine, Mem. 11, Pau. Waller, H. O. and W. Polski. 1959. Planktonic foraminifera of the Asiatic shelf. Contr. Cushman Found. Foram. Res. 10(4): 123-126. Walton, W. R. 1964. Recent foraminiferal ecology and paleoecology. Pages 151-237 in John Imbrie and Norman Newell, eds. Approaches to paleoecology. John Wiley and Sons, Inc., New York, 31 figs. Wang, P. et a1. 1984. Marine micropaleontology of China. China Ocean Press, Beijing. 370 pp., 38 pis. Weng, X. and C. Wang. 1984. A preliminary study on the T-S characteristics and the origin of Taiwan Warm Current water in summer. Studia Marina Sinica 21: 113-133. 212 BULLETIN OF MARINE SCIENCE, VOL. 47, NO. I, 1990

Zheng, S. 1979. The Recent foraminifera of the Xisha Islands. Guangdong Province, China II. Ibid. 15: 101-232, pis. 1-27. ---. 1980. The Recent foraminifera of the Zhongsha Islands, Guangdong Province, China I. Ibid. 16: 143-182, pis. 1-8. ---. 1988. The agglutinated and porcelaneous foraminifera of the East China Sea. Science Press, Beijing. 425 pp., 87 pis., 125 figs. --- and Z. Fu. 1988. The distribution of agglutinated foraminifera in the East China Sea. Revue de Paleobiologie, vol. spec. No.2, Benthos, '86, pp. 929-949. Zheng, Z., S. Zheng and Z. Fu. 1979. Preliminary faunal analysis of the foraminifera of the East China Sea. Kexue Tongbao no. 19, pp. 903-906.

DATE ACCEPTED: March 5, 1990.

ADDRESS: Institute of Oceanology, Academia Sinica, No. 7 Nanhai Road, Qingdao (Postal Code: 266071), Shandong Province, The People's Republic of China.