2 Department of Earth System Science, Ministry of Education Key Laboratory for Earth System Modeling, Tsinghua University, Beijing 100084, China;
3 School of Life Sciences, Xiamen University, Xiamen 361102, China
The genus Azpeitia was created and discussed in detail by Peragallo from the Osuna-Seville (Spain) fossil material (Tempère and Peragallo, 1915). Originally, Azpeitia Peragallo was described as a monotypic genus, with its type species being A. antiqua. Many of the species belonging to Azpeitia were originally placed in Coscinodiscus (Fryxell et al., 1986). According to Fryxell et al. (1986) the genus Azpeitia is characterized by valves with a nearly central rimoportula, often on the edge of an annulus; a ring of rimoportulae on the edge of the valve mantle; specialized areolae patterns on the mantle differing from those on the valve face; and two or more hyaline girdle bands including a wide valvocopula. There are 26 named species in Guiry and Guiry (2018) at present, as well as 4 infraspecific names. Of the species names, 23 have been accepted taxonomically. Fryxell et al. (1986) described A. africana and A. barronii. Almost all Azpeitia species have a warm water distribution in tropical/subtropical waters (Fryxell et al., 1986; Shiono and Koizumi, 2002; Seeberg-Elverfeldt et al., 2004; Jiang et al., 2006; Barron and Bukry, 2007; Garcia and Odebrecht, 2012; Barron et al., 2014; Chakraborty and Ghosh, 2016). The only exception is A. tabularis, which has radiated into austral cold water masses and is especially abundant in the Subantarctic Zone northwards and southwards of the Antarctic Convergence, although it is uncommon near ice (Fryxell et al., 1986; Garcia and Odebrecht, 2012; Ren et al., 2014). Ren et al. (2014) reported the distribution of A. tabularis in the North Pacific Ocean where summer sea surface temperatures ranged from 7℃ to 27℃.
Azpeitia includes fossil and living marine species, ranging from the Eocene to the Recent. Most species are found in the middle Miocene, and only six extant species have been found: A. africana, A. barronii, A. endoi, A. neocrenulata, A. nodulifera and A. tabularis (Fryxell et al., 1986; Garcia and Odebrecht, 2012).
Because A. africana, in common with other members of Azpeitia, has an external cribrum, an internal foramen, rimoportula positioned on the edge of a central annulus, and a marginal ring of rimoportulae, Fryxell et al. (1986) transferred A. africana from Coscinodiscus. A. africana is common in equatorial and tropical marine waters (Fryxell et al., 1986; Jiang et al., 2006; Garcia and Odebrecht, 2012). It has been reported that A. africana has an occurrence range from the Late Pleistocene to Recent in the South China Sea (SCS) (Lan et al., 1995) and it commonly appears in SCS surface sediments (Jiang et al., 2004, 2006). However, the morphological description of A. africana in the SCS is inadequate, as is the original description, and the fine structure has not been observed at all with EM. Therefore, the morphological structure and distribution patterns of A. africana in SCS surface sediments remain unclear. The present paper studies the morphological structure and variability of A. africana and determines its geographical distribution in SCS surface sediments, increasing our knowledge of marine diatom diversity and ecological distribution information in the SCS, and providing essential information for paleoceanographical reconstructions of the SCS.2 MATERIAL AND METHOD 2.1 Sampling and sample processing
We studied the morphology and distribution of the marine diatom A. africana from 62 samples in the uppermost 1 cm of sediment in the SCS. The sediment samples were collected with a grab or a box corer during cruises on R/Vs Ocean-4 in 2000–2001, Shiyan-3 in 2007 and Yanping-2 in 2007. The sampling stations were located between 3°56.61′-20°59.37′N and 108°30.68′–116°46.70′E (Table 1, Fig. 1). The water depths of sampling stations ranged from 72 m to 4 238 m. Optical microscope samples were prepared according to Håkansson (1984). Samples were treated with 10% HCl to remove calcareous matter and then treated with 30% H2O2 (1–2 h in a water bath at 60℃) to remove organic material. Samples with high proportion of clay were washed repeatedly by suspending and dispersing the material in distilled water in a 100-mL beaker. The supernatant was decanted off after at least 3 h, and the aliquot of the suspension was shaken, smeared on a cover slip and dried. After the materials were completely dry, samples were mounted with Naphrax. Samples for scanning electron microscopy (SEM) were prepared according to Huang et al. (1998). The coverslip was placed in dilute sulfuric acid and boiled for 30 min, then soaked in alcohol for 1 week. The sample liquid was dropped on a coverslip, and the sample was observed under the JEM-100CX Ⅱ SEM (JEOL, Akishima-shi, Japan) after sputtering with gold for 25–30 s.2.2 Diatom data processing
Diatoms were identified and counted with an Olympus BX-51 (Olympus, Tokyo, Japan) microscope using phase contrast at a magnification of 1 000×. The fine structure of A. africana was observed using a JEM-100CXII scanning electron microscope. The absolute number of diatom valves per gram of sediment was calculated as:
number of valves/g=((N×(S/s))×(V/v))×1000/w,
where N is the number of diatom valves observed; S is the total number of separated rows per slide; s is the number of rows in which diatoms were counted; V is the total volume; v is the volume of solution placed onto cover slip; and w is the dry weight of the sample. Relative abundances of individual taxa are given as percentages (Abrantes et al., 2007).3 RESULT 3.1 Morphology
Azpeitia africana (Janisch ex Schmidt) G. Fryxell & T. P. Watkins (Plate Ⅰ)
Coscinodiscus africanus Janisch ex Schmidt, Atlas der Diatomaceenkunde 15, pl. 59, figs. 24, 25.1878; Jin et al., 1982, p. 28; Fryxell et al., 1986, p. 19, figs XVII, XVIII SEM; XXXII-1, 2 LM; Lan et al., 1995, p. 16, pl. 5/28, 29; Guo et al., 2003, p. 83, Fig. 52.
Description: The valve is disc-shaped, flat, with radial areolae in decussating arcs and diameters of 30–95 μm. There is an eccentric ring with areolae arranged in lines near the center of the valve; areolae radiate from this eccentric ring rather than from the geometric center of the valve; 4–6 areolae in 10 μm (Plate Ⅰa). There are between 8 and 10 marginal striae in 10 μm. A rimoportula is located on the edge of the eccentric ring of areolae proximal to the geometrical center of the valve, with its slit aligned with a radial row of areolae (Plate Ⅰa, b). This nearly central rimoportula, with an external tube, is recessed externally and is somewhat more flared than the marginal rimoportulae (Plate Ⅰa, b). The marginal rimoportulae are not evenly spaced with 3–8 μm apart, more closely appressed in one quadrant of the valve (Plate Ⅰa, b, c). A curved external slit leads to each marginal rimoportulae. The slits begin in opposite directions at the midpoint of closely packed processes, 180° from that point, and they meet on the side of the valve, facing the same direction (Plate Ⅰd). Fryxell et al. (1986) term these poles "the 0° point" and the "180° point"; these slits spiral away from the "0° pole" and toward the "180° point". In addition, the marginal rimoportulae are not evenly spaced but are denser in a sector defined by the plane through the "0° pole" and "180° point" poles and the nearly central rimoportula (Plate Ⅰd, e, f). This uneven distribution also lends polarity to the valve.3.2 Geographical distribution of A. africana in the SCS
Diatom valve abundance and the relative abundance of A. africana (percentage contribution of A. africana to total diatom valve abundance) are shown in Table 2 and Fig. 1. It was shown that A. africana is abundant and widely distributed in the SCS, being observed in samples from 43 of the 62 stations, an occurrence rate of 69.4%. The relative percentage of A. africana to total diatom cell abundance was high, with a maximum value of 8.1% in Station NS2007-22.
Azpeitia africana was more abundant in the southern region of the SCS, and was concentrated in the area 7°48.56′–9°58.40′N, 113°22.29′–116°46.70′E. Its abundance accounted for 0.9%–5.6% of all species in the Xisha Islands area. The lowest abundance of A. africana (0%–2.5%) was in the northern regions of the SCS and the Sunda Shelf, areas easily affected by coastal currents because of the shallow depth. The species was not detected on the northwestern continental shelf (shallow water area) and northern Kalimantan Island shelf (SA09-087, SA09-089, SA09-091, SA09-098, SA09-100).4 DISCUSSION 4.1 Morphological characteristics of A. africana
Azpeitia africana was originally described as the new species Coscinodiscus africanus by Janisch ex Schmidt (1874–1859). According to Janisch ex Schmidt, it was distinguished by "an eccentric" structure in valve. The "an eccentric" in valve is inferred to be the external opening of central rimoportula near the valve center. Hustedt (1928) also reports A. africana (as C. africanus) that shows a large, coarse valve with radial rows of areolae of irregular sizes but with the larger ones in the middle of a radius. Marginal processes were shown, with diameters of 30–90 μm, 6 areolae in 10 μm, marginal processes 5–6 μm apart, and 8 striae in 10 μm at the margin. Simonsen (1974) shows that marginal processes are not evenly spaced, the slits start in opposite directions at the midpoint of closely packed processes and they meet on the opposite side of the valve, facing the same direction. Fryxell et al. (1986) make the new combination A. africana from all Gulf Stream warm core rings, moving it out of the genus Coscinodiscus. Diameters given for A. africana by Fryxell et al. (1986) are 33–76 μm, a narrower range than that observed in our sample materials (which are 30–95 μm). Whereas Fryxell et al. (1986) report 5–10 areolae in 10 μm, we found a range of 4–6 areolae in 10 μm. They report the distance between the two marginal rimoportulae as 3–6 μm, but we found a larger variation of 3–8 μm. The marginal striae (8–10 in 10 μm) were the same as Fryxell et al. (1986) describe. Fryxell et al. (1986) find that the genus Azpeitia has five living species; however, there is a distinct difference between A. africana and the other living species of Azpeitia.
In the living species, A. africana is very similar to A. barronii. They have unevenly spaced marginal rimoportulae positioned closer together in one quadrant than in the others. Fryxell et al. (1986) think that this character is of more recent origin than in the previously mentioned Azpeitia species (A. tabularis, A. neocrenulata, A. nodulifer, A. barronii). The patterns on the processes of A. africana as seen from the inside are similar to those of A. barronii: one large central rimoportula with an external tube adjacent to the center. In these two species, the external openings of the labiate processes are elongated slits with siliceous elaborations. Although the geographical distribution of the two species is similar (both are found in warm marine waters), there are distinct morphological differences between A. africana and A. barronii (Table 3).
According to Fryxell et al. (1986), this species is similar to A. tabularis. In these two living species, the external opening of the nearly central rimoportula is reduced. A. tabularis has the opening flush with the internal areola walls, and the external opening of the central rimoportula has little or no external projection. A. africana has a recessed opening. The areolae of A. africana are very similar to those of A. tabularis, sometimes partly occluded by radial threads, forming a basket-shaped covering. They differ in that A. africana is a warm water species, while A. tabularis is a cold-water species.4.2 Ecology and distribution of A. africana
Azpeitia africana is a warm water, marine planktonic species found in most surface sediment samples collected from the stations in the SCS. The water depths ranged from 72 m to 4 238 m. It was recorded as C. africanus in Late Quaternary sediments from the SCS (Lan et al., 1995), and in surface sediments from the SCS (Jiang et al., 2004). It was recorded as C. africanus in the East China Sea (ECS) (Liu, 2008), and Jin et al. (1980) described C. africanus as a representative species in the ECS. In addition, Fryxell et al. (1986) found it in all warm Gulf Stream cores, as well as in plankton tows from the Central Pacific and Gulf of Mexico. Azpeitia africana is also often recorded from fossil material, from the upper Pliocene to Holocene sediments in the tropical Eastern Pacific (Barron, 1980). Burckle (1978) correlates the first occurrence of A. africana (C. africanus) with the late early Pliocene. It is also found in North Atlantic sediments (Baldauf and Barron, 1982) and Indian Ocean sediments (Schrader, 1974).4.3 The environmental significance of A. africana
Previous studies have shown that A. africana is typical of tropical planktonic diatoms, widely distributed in the Western Pacific (Jousé et al., 1969) and Eastern Pacific (Jousé et al., 1971). The diatom complexes in the surface sediment layer of the Pacific Ocean can be divided into Arctoboreal diatom complex, Northboreal diatom complex, Subtropical diatom complex, Tropical diatom complex, Equatorial diatom complex, Subantarctic diatom complex and Antarctic diatom complex. Of these, the Tropical diatom complex and Equatorial diatom complex may reflect the characteristics of diatoms found in the North Equatorial Current and its branch, as well as in the Kuroshio Current (Jousé et al., 1971). The main composition of the Equatorial diatom complex in this research comprised A. africana, which was widely distributed in surface sediments in the SCS (Jiang, 1987; Jiang et al., 2004; Ran and Jiang, 2005), as well as in the areas of inflow of the warm Kuroshio Current in the ECS (Jin et al., 1980).
Ran and Jiang (2005) showed that there was a higher content of A. africana in the northeastern area of the SCS, where it accounts for 5% of diatom abundance. In the central and southern areas of the SCS, A. africana content was about 2.33%–4.10% of diatom abundance and the lowest percentage (0%-1.71%) was in the western and southeastern regions. Similarly, our results show that A. africana had the highest value of relative valve abundance in the southern area of the SCS, reaching 0.9%–5.6%. In our research, A. africana was more abundant in the southern region of the SCS, concentrated in the area of 7°48.56′–9°58.40′N, 113°22.29′–116°46.70′E. Azpeitia africana can be used as an indicator of the intrusion of the Kuroshio Current and Indian Ocean water (Ran and Jiang, 2005). As an indicator species, A. africana is prevalent in the area of the Kuroshio Current in surface sediments, indicating that its distribution is not only affected by the waters of the SCS, but also by those of the ECS (Jin et al., 1980). The climate and surface-water circulation in the SCS were largely controlled by monsoons driven by differential warming in adjacent continents and oceans (Wytki, 1961), resulting in abnormal rain and wind in the summer and winter of monsoon years. The northeast and southwest monsoons change the surface-water circulation regularly, bringing water into the SCS from the Western Pacific, including probably the warm Kuroshio Current (Wytki, 1961) through the Bashi Strait north of Luzon, and Indian Ocean surface water across the Sunda Shelf in summer (Wang and Abelmann, 2002). In this study, A. africana was shown to be a widely distributed species in the SCS, and its relative abundance was relatively higher in the southern region of the SCS. This may be attributed to the effect of the southwest monsoon which prevails during the summer, from the Java Sea to the south tropical Indian Ocean waters through the Cary Mata Strait, Gaspar Strait and the Malacca Strait, and into the SCS through the Sunda Shelf.
Our results suggest that the warm water planktonic species A. africana could be used as a good indicator of the intrusion of the Kuroshio Current and Pacific Ocean warm water in paleoenvironment reconstruction, and also support previous studies on the environmental indicators of A. africana.5 CONCLUSION
This study observed the morphological features of the marine diatom A. africana from the SCS by LM and SEM. The main morphological characteristics of A. africana are: the valve is disk-shaped, with an eccentric ring of almost linear areolae near the center of the valve, the lines of areolae radiating from the eccentric ring. A central rimoportula has an external tube recessed on the edge of a central ring. The marginal rimoportulae are not evenly spaced, and are positioned closer together in one quadrant than in the others.
Our studies on the geographical distribution and ecological characteristics of A. africana have shown that this tropical planktonic species was the dominant diatom throughout the SCS, although its distribution was uneven. A. africana was more abundant in the southern region of the SCS and the Xisha Islands area, and was in low abundance or even absent in the shallow water area of the continental shelf and northern Kalimantan Island shelf. In paleoceanographic reconstructions of the area, A. africana may be used as an ideal indicator of the warm Pacific Ocean water, including the Kuroshio Current flowing into the SCS. Our results have provided a basis for further paleoceanographic research in the SCS.6 DATA AVAILABILITY STATEMENT
The data sets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.7 ACKNOWLEDGMENT
We thank Elaine Monaghan BSc(Econ), from Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.
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