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Article

Distribution and Environmental Impact Factors of Picophytoplankton in the Eastern Indian Ocean

by
Xingzhou Wang
1,2,
Feng Wang
3 and
Jun Sun
2,4,*
1
College of Food Science and Engineering, Tianjin University of Science and Technology, Tianjin 300457, China
2
Research Centre for Indian Ocean Ecosystem, Tianjin University of Science and Technology, Tianjin 300457, China
3
Jiaozhou Bay Marine Ecosystem Research Station, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
4
College of Marine Science and Technology, China University of Geosciences, Wuhan 430074, China
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2022, 10(5), 628; https://doi.org/10.3390/jmse10050628
Submission received: 11 April 2022 / Revised: 29 April 2022 / Accepted: 1 May 2022 / Published: 5 May 2022
(This article belongs to the Section Marine Ecology)
Browse Figures
Versions Notes

Abstract

:
Picophytoplankton (pico) in the eastern Indian Ocean (EIO) were investigated during the inter-monsoon periods. They were found to typically comprise Prochlorococcus (Pro), Synechococcus (Syn), and Picoeukaryotes (PEuks). In the survey area, the pico showed two different vertical distribution patterns in different regions, whereby the Syn abundance decreased with depth, whereas those of Pro and PEuks increased and then decreased with depth, with the maximum depths ranging from 50 to 100 m. The cell abundance and community structure of the pico were similar at the equator (EQ) and the eastern boundary of the Indian Ocean near Sumatra (EB), but the pico cell abundance was significantly lower in the Bay of Bengal (BOB). Pro dominated most regions of the entire EIO and were approximately one-to-two orders of magnitude more abundant than Syn and PEuks. The distributions of Syn and PEuks showed little difference across various regions. Influenced by the physicochemistry of circulation and water masses, there were many different environmental factors in the different regions. The abundance of pico domination by Pro showed a strong positive correlation with the nutrients and salinity in the survey area, indicating increasing nutrient availability, particularly in the oligotrophic EIO. Generalized additive models (GAMs) analysis showed the differences in their responses to environmental variability. Pro and PEuks both increased strongly with warming up to below 26 °C, and Pro and PEuks were more responsive to chemical (nutrient) variability. Syn showed a broader tolerance of low-salinity conditions. In a certain range, an increase in nitrite and nitric acid can improve the cell abundance of Pro. As a significant contributor to primary productivity in oligotrophic waters, this study provides essential information for studying pico communities in the EIO and its adjacent marine ecosystems.

1. Introduction

As a significant contributor to the primary productivity of marine ecosystems [1], phytoplankton are widely distributed in the euphotic layer of the ocean [2]. Phytoplankton can be divided into three categories according to their size: microphytoplankton (20–200 μm), nanophytoplankton (2–20 μm), and picophytoplankton (0.2–2 μm) [3,4]. Picophytoplankton (pico), the group with the smallest members, has become a focus of marine science since its discovery. Although the conditions in the tropical and subtropical oligotrophic seas are not suitable for the growth of larger phytoplankton due to nutrient restrictions, the biomass and productivity of Synechococcus (Syn) [5] and Prochlorococcus (Pro) [6] are very high, and they account for 60%~80% of the total phytoplankton biomass [7,8]. Syn is distributed in the world’s oceans and plays a key role in marine food webs and energy flow due to its extensive adaptability. Pro has an absolute advantage in the ocean due to its small cell size and ability to survive at low nutrient concentrations [9,10]. The abundance of Pro in the open ocean is usually 10 times or more than that of Syn [11]. Picoeukaryotes (PEuks) are widely distributed in the global oceans of tropical, temperate, and cold regions due to their strong adaptability to temperature [12,13,14]. Due to slow sinking and more efficient nutrient utilization and carbon fixation, Pro has a high cell abundance, has a wide distribution, and plays a key role in marine ecosystems and carbon cycling [15,16,17]. Pico has a significant impact on the global biogeochemical cycle [18]. Biological particle size can reflect the biomass, energy, and other relations of different trophic levels. Classifying phytoplankton by particle size is a convenient method for quantitative research on the matter and energy cycle and plankton dynamics of the ecosystem [19]. The high abundance, wide distribution, and high primary production of pico all have profound effects on marine ecosystems and biogeochemical cycles. Therefore, revealing their biogeographic patterns is crucial in order to understand the contribution of different regions to the carbon cycle of these particular groups.
As a part of the global ocean cycle, the eastern Indian Ocean (EIO) is bounded by the Indian subcontinent to the north, the Arabian Sea to the west, and the Indonesian islands to the east, being second only to the Western Pacific Warm Pool [20]. Influenced by the topography, the interaction between the cold air from the Himalayas and the warm and humid airflow from the Indian Ocean causes the region to have an obvious monsoon climate [21,22]. In the spring monsoon period, the vertical mixing in this area is weak [23], which causes the mixing layer to move upward, and the nutrients available for phytoplankton decrease [24]. Affected by monsoon and ocean currents, the primary productivity in the EIO is low [25]. Compared with the Pacific and Atlantic Oceans, the pico in the EIO exhibit complicated regional distribution [26]. To more clearly understand the pico ecosystem, we compared the composition and structure of the pico in different environments in the EIO to better understand the dynamics and regulatory mechanisms of pico in such ecosystems. At the same time, the structure and dynamics of the three groups, together with the related hydrological and physicochemical conditions, were analyzed to understand the factors affecting the distribution of these pico in EIO.

2. Methods

2.1. Study Area

Water samples were collected in a cruise of R/V Shiyan III from February to April 2017 from 21 sampling stations (Figure 1). At each station, seawater samples were collected from seven discrete depths within the water column using a rosette sampling system equipped with SeaBird CTD (conductivity, temperature, and depth; SBE 19 Plus). Temperature, salinity, and depth were simultaneously recorded online.

2.2. Sampling and Analysis

FCM (Becton-Dickinson Accuri C6) can effectively detect and enumerate the pico groups without the need for fluorescence staining [27], and it is considered to be very successful in the studies of pico [28]. Seawater (1.5 mL) was taken at the corresponding depth at the survey station, and 0.5 mL of paraformaldehyde was added. Then, only 196 μL seawater was used for analysis at a speed of 66 μL/min for 3 min. The sample injection chamber volume allows for a direct cell count per μL. After melting the frozen sample, part of each sample was combined with YG fluorescent (1 μm; Polysciences) pellets as an internal reference and then analyzed with flow cytometry (Becton-Dickinson Accuri C6). Three taxa of pico were divided and counted by the two-parameter graph of forward scatter light (SSC), orange fluorescence (FL2, 585 ± 40 nm), and red fluorescence (FL3, >670 nm; FL4, 675 ± 25 nm) [29].
In situ seawater was filtered through a 0.45 μm cellulose acetate membrane and then refrigerated at 4 °C for nutrient analysis in the laboratory. Technicon AA3 Auto-Analyzer (Bran + Luebbe) was used to detect ammonium, nitrate, phosphate, and silicic acid salts. Copper–cadmium column reduction and indophenol blue spectrophotometry were used to analyze nitrate and ammonium concentrations. Typical spectrophotometry was used to analyze dissolved inorganic silica (DSi) and phosphorus (DIP) [30,31,32]. The concentration of chlorophyll-a (Chl-a) was determined using the extraction fluorescence method. Samples were collected by filtration of 1 L seawater using GF/F filters (0.7 μm porosity). Chl-a analysis using a diaphragm vacuum pump under a vacuum of less than 100 mm Hg. The filter was placed into a 10 mL brown glass tube, then 5 mL of acetone with a volume fraction of 90% was added to the glass tube and stored in the dark at 4 °C for 24 h. The Chl-a fluorescence was measured in non-acidified mode using the Turner Fluorometer (model 10-AU) and calculated according to the formula reported by Parsons [33].

2.3. Data analysis

The abundance of phytoplankton cells in the water column is calculated by the trapezoidal integral method [34]:
P = ∑ i = 1 n − 1 P i + 1 + P i 2 D i + 1 − D i / D
where P is the average of phytoplankton abundance in the water column, Pi is the abundance value of phytoplankton in layer i, D is the maximum sampling depth, Di is the depth of layer i, and N is the sampling level.
The relationship between pico and environmental factors was analyzed using Redundancy analysis (RDA; Canoco 4.5). Figures depicting horizontal and vertical phytoplankton distributions were constructed using Ocean Data View 4.10, Original 8.5, ArcGIS 10.2. We constructed generalized additive models (GAMs) using the R package “mgcv” to fit the responses of temperature, salinity, nitrite, and nitrate to the abundance of pico.

3. Results

3.1. Hydrographic Conditions

The distributions of weighted average temperature and salinity in the survey area are shown in Figure 2a,b. There were obviously high temperatures and low salt at 10° N. In the vertical distribution, temperature decreases with depth, and salinity increases from the surface to the bottom (Figure 2c,d). The 10° N thermocline was deeper, and the salinity was lower at 10° N above 75 m (Figure 2c,d). High surface temperature and salinity were particularly observed near the equator between 80 and 90° E due to the apparent influence of the Wyrtki jets (WJ). The equator had a markedly high salinity zone. Based on temperature and salinity distributions, the sampling stations were divided into three subregions (Figure 1), namely the Bay of Bengal (BOB), the equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
There were obvious regional differences in Chl-a and nutrients, and the maximum value of Chl-a appeared at 50–100 m depth in the surveyed area (Figure 3f). The concentration of Chl-a in BOB was higher than that in EB and BOB. In terms of vertical distribution, the concentrations of all nutrients above 75 m were relatively low and gradually increased with increasing depth. The concentrations of nutrients in BOB and EB were significantly higher than in EQ (Figure 3a–e), indicating that the nutrients may be supplemented by the marginal sea, which usually serves as a nutrient sink. The distribution of nutrients was similar to that of temperature. Overall, the environmental factors of BOB were significantly different from those of the EQ and EB. The nutrients of BOB were affected by upwelling and the input of nearshore nutrients, and the concentration of nutrients was significantly higher in BOB than in the other two regions. The distribution of temperature and salinity differed in the Indian Ocean. Due to the influence of diluted water, BOB had low salinity. Influenced by the Wyrtki jets, the salinity of EQ was significantly higher than of BOB and EB. The main area influenced by the Wyrtki jets is 60 to 90°E. The Wyrtki jets move from west to east, bringing high temperature and high salinity water and gathering in the east, which changes the eastern sea’s temperature and salinity. The temperature and salinity of EB show very little change. The thermohaline and halocline in the survey area range from 50~100 m. The distribution of nutrients is similar to that of thermocline and halocline. The nitrite in BOB is significantly different from that of the other two regions.
We compared the N:P, Si:P, and Si:N ratios in the surface, middle, and bottom layers. Nutrient concentrations in the surface layer were lower. N:P and Si:P ratios in BOB show that phosphorus is limited (N:P > 16, Si:P > 15). Nutrients were changed in the middle layer, whereby nitrogen, phosphorus, and silicon were no longer biological limiting factors. The depth continued to increase to the bottom, and the ratio of nutrients was maintained in a stable range. At the bottom, the abundance of phytoplankton decreases, interspecific competition decreases, nutrient ratios stabilize, and phytoplankton growth is limited by light. The limitation of phosphorus was more pronounced in the surface layer of BOB than in the other two regions, and the nutrient ratios showed more volatility in EQ (Figure 4). Three regions showed more consistency in the middle and bottom layers, where the nutrients were not the limiting factor for phytoplankton growth.

3.2. Distributions and Compositions of Pico Abundance

The vertical distribution of Syn, Pro, PEuks, and pico are shown in Figure 5. The cell abundance of Syn ranged from 4.76 × 101 to 1.06 × 104 cells/mL, with an average of 2.59 × 103 cells/mL. The cell abundance of Pro ranged from 5.44 × 101 to 1.17 × 105 cells/mL, with an average of 1.23 × 104 cells/mL. The cell abundance of PEuks ranged from 6.80 to 5.04 × 103 cells/mL, with an average of 7.26 × 102 cells/mL. The abundance of Syn was lower in I210 near Sri Lanka (Figure 5a). The cell abundance was high at two sites along the coast of Indonesia. Pro and PEuks have similar horizontal distribution and higher cell abundance in the open ocean. The cell abundance of Pro occupies an absolute advantage in each survey station (Figure 5b). The maximum cell abundance of the Pro was between 50 and 100 m (Figure 5b). For the distribution of Syn, no obvious distribution pattern was observed. Syn in the upper layer was slightly higher than in the lower layer (Figure 5a). The abundance of Syn in the BOB and EB was higher than EQ. The vertical distribution of Pro and PEuks were similar (Figure 5b,c), showing a trend of a gradual increase from 50 to 100 m depth and then a decrease.
The average abundance of pico was calculated for the three regions at different depths. In the three regions, Pro dominates the distribution of pico, especially at 75 m (Figure 6a–c). In the EIO, the abundance of Pro was approximately 1–2 orders of magnitude higher than Syn and PEuks. In EB and EQ, the vertical distribution and abundance of pico were similar. The largest cell abundance occurred in the middle layer of EQ and EB, and the cell abundance in Pro was significantly higher than that in PEuks. The vertical distribution of pico showed a similar trend to that of Pro.
In our study, we used the water column integral to calculate the average abundance of pico above 200 m because of the inhomogeneous vertical distribution. The abundance and percentage of pico above 200 m are shown in Figure 7. The difference in abundance was small at most stations. However, the abundance of nearshore pico was lower, for example, at stations I210 and I304. The station with the lowest average abundance was I210, and the station with the highest average abundance was I708. Pro was dominant in each station (Figure 7). Comparing the mean cell abundance of subregions and the percentage of each species, BOB had a lower mean cell abundance than the other two regions, while the percentage of Syn was higher in BOB (Figure 7b).

3.3. Relationship between Pico Abundance and Environmental Factors

Redundancy analysis (RDA) (Figure 8) was carried out to deduce the interrelations between response and explanatory variables. Figure 8 depicts the percentage variance of species data in two axes (65.1%). Temperature, salinity, nitrite, and nitrate (p < 0.01) contributed significantly to the total variance of the survey area (Figure 8). Syn was negatively correlated with major nutrients and positively correlated with temperature and ammonium, and Pro and PEuks were positively correlated with nitrite. This indicates that temperature is the main factor affecting the distribution of Syn, while the distribution of Pro and PEuks is greatly affected by nitrite.
In our GAMs, temperature, salinity, nitrite, and nitrate were strong predictors of Syn, Pro, and PEuks. Comparing the trend of Syn with temperature, the effect of temperature on Pro and PEuks was more obvious (Figure 9a,e,i). Syn had better adaptability under low nitrate concentration, and Pro and PEuks show an obvious peak with the increase in nitrate. However, Pro and PEuks decreased rapidly with increasing nitrate, while Syn decreased more slowly (Figure 9c,g,k). The abundance of Syn decreased gradually with the increase in nitrite, while the abundance of Pro and PEuks increased with the increase in nitrite (Figure 9d,h,l).

4. Discussion

4.1. Characteristics of Pico Vertical Distribution

Pico typically dominate in low-latitude open-ocean ecosystems [35] under conditions of higher irradiance, higher temperature, enhanced stratification, and oligotrophy. At temperatures below 26 °C, both Syn and Pro were positively correlated with temperature. Pro and PEuks, however, showed a higher rate of change. Above 26 °C, Pro showed a negative correlation, while Syn still showed a positive correlation. Salinity has a more pronounced impact on Pro than Syn, whereby elevated salinity inhibits Syn and promotes Pro. In addition, the different trends of Pro and Syn with very low but increasing concentrations of nitrite and nitrate suggest a strong advantage for Pro in oligotrophic waters of improving nutrient status, but the range is very small.
Natural ecological studies have shown that the maximum abundance of Pro on the water column generally occurs near nitrite [35,36,37]. The RDA revealed that the distribution of Pro was closely related to nitrite. Ammonium and nitrite can be used as the main nitrogen sources for Pro around 75 m depth. The reported temperature was less than 26 °C, close to the ecological threshold essential for Pro growth, which is in accordance with our results. The maximum abundance of Pro in the water column appeared near the thermocline in the oligotrophic sea area (Figure 2, Figure 3, Figure 4 and Figure 5). PEuks had a larger range of adaptation to light and more diverse physiological types and gene diversity [38,39]. Therefore, PEuks are widely distributed in the world’s oceans, and a high abundance of PEuks cells has been detected in environments low in light and high in nutrients. Light intensity is not one of the most important factors limiting the abundance and spatial distribution of PEuks cells. In our results, PEuks are negatively correlated with depth and positively correlated with temperature. PEuks have obvious biogeographical distribution characteristics, such as environmental filtration, niche differentiation, or diffusion limitation [40].
Studies have shown that the growth of PEuks is greatly restricted by nutrients. High cell abundance was more frequently observed in low irradiance but high nutrient environments [39]. In our survey, the vertical distribution of PEuks is similar to that of Pro, and the maximum abundance appears near the thermocline. To assess the contribution of microplankton to phytoplankton, we compared cell abundance with total chlorophyll based on flow cytometry, because of the high specificity of diagnostic pigments for Pro and PEuks (Figure 10, higher R2). We believe that Pro contributes the majority of phytoplankton biomass in the eastern Indian Ocean.

4.2. Coupling of Hydrography and the Pico Community

It is well known that the EIO has a complex hydrological environment. The northern part of the survey area is characterized by significantly lower salinity, which is primarily influenced by dilution due to water from the BOB [41]. The high levels of salinity were particularly observed between 80 and 90° E around the equator. This is probably because the Wyrtki jets are strongest between 60 and 90° E. As the water moves, high-salinity water gradually accumulates in the east, resulting in higher salinity and further affecting the water structure in the region. At the same time, there is influence from the upwelling off Sumatra, resulting in higher salinity near EB. These factors result in the differences in environmental factors in the investigated regions, and in particular, in the surface layer of BOB, temperature, salinity, and phosphate showed obvious differences (Figure 2 and Figure 3). In the marine ecological environment, nutrients are an important determining factor of the phytoplankton community. Our survey area had strong stratification, whereby the vertical stratification of the survey area determines the distribution of environmental factors, such as nutrients, and then influences the community structure of phytoplankton. In our study, N:P > 16 in the surface layer of BOB, which indicates this region is phosphorus-limited, N:P < 16 in the surface layer of EQ, and N:P = 16 in the surface layer of EB. As the depth further increases, the nutrient concentration increases, and the N:P in the middle and bottom layers is relatively stable (N:P < 16). With further increase in the depth, the nutrients in the bottom layer also gradually increase. Pico showed two distinct vertical distribution characteristics in the survey area. The abundance of Syn decreased with increasing depth. Both Pro and PEuks reached the maximum abundance at 75 m (Figure 5).
Studies have revealed that Pro is commonly found in the oligotrophic environments of subtropical and tropical oceans and is limited by low temperature at high latitudes by environmental factors in coastal waters and upwelling areas such as limited nutrient availability, heavy metal toxicity, and competition among groups [42,43]. In our correlation analysis, we found that the Pro distribution is positively correlated with nitrite and salinity. Pro is smaller in size and has a greater nutritional competitive advantage compared to other microorganisms, with higher cell abundance in the oligotrophic waters of the open ocean. Temperature and salinity are considered key ecological determinants of Pro [44]. In our study, salinity played an important role in the pico abundance, and river input may inhibit Pro growth [45].
At the same time, the depth of Pro maximum concentration is positively correlated with the nutrient concentrations. Pro with low light adaptation has a nitrite absorption gene so that nitrite can be used as the main nitrogen source of Pro near the halocline. Therefore, high salinity and nitrite were the main reasons for the higher cell abundance of Pro in the EB and EQ than in the BOB. In the investigated area, the cell abundance of pico was significantly lower in BOB than in the other two regions. The most obvious feature was that the abundance of Pro was significantly lower than in the other two regions; this is similar to the results of Wei [18]. Syn abundance is similar in different regions, where Syn showed negative correlations with nutrients, nitrate, silicate, and phosphate in EQ and EB. Our results show that ammonium significantly promotes the cell growth of Syn, which is in agreement with previous field investigations reported by Glibert and Lindell [46,47]. Syn can utilize various urea, amino, and nitrogen as nitrogen sources [48,49].
It should be noted that Syn showed a strong positive correlation with temperature in different regions, but temperature, salinity, light, and nutrient changes are closely related to depth. The investigation area was mainly affected by diluted water, but due to faring from the estuary, the water body shows little influence by light. PEuks have a strong ability to adapt to the environment and are distributed in both oligotrophic sea areas and polar regions, but low nutrient concentrations limit PEuks growth [50]. Our results also show that PEuks have a significantly positive correlation with nitrite. Therefore, the lowest cell abundance of PEuks observed in the EIO is mainly attributed to the nutrient restriction. Our RDA and GAMs were constructed to fit field data on biomass rather than growth rate potential. The results reflect the net differences in the trophic interactions of photosynthetic bacteria and their physiological responses [35]. Our results support the idea that compared with Syn, Pro will benefit more from higher temperature, increased stratification, and lower nutrients expected to result from global warming.

5. Conclusions

The distribution of pico in the EIO was found to depend on Pro, followed by Syn and then PEuks. The vertical distribution of pico in different regions was similar, but under the effect of environmental factors, Pro levels of 50–75 m were significantly lower in the BOB than in the EQ and EB. Salinity and nitrite played a key role. Although Pro showed significant changes in cell abundance in the survey area, the absolute abundance of Syn and PEuks was similar, so the question of whether there is an interaction between pico communities and their mechanism needs to be further explored.

Author Contributions

Conceptualization, J.S.; Data curation, X.W.; Formal analysis, X.W.; F.W.; Funding acquisition, J.S.; Investigation, X.W.; Resources, J.S.; Supervision, J.S.; Writing—original draft, X.W.; Writing—review and editing, J.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the National Nature Science Foundation of China grants (41876134 and 41676112), the Changjiang Scholar Program of the Chinese Ministry of Education (T2014253) to Jun Sun, and the State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (No. GKZ21Y645).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are available from the authors upon request.

Acknowledgments

The authors would like to thank the Open Cruise Project in the Eastern Indian Ocean of the National Nature Science Foundation of China (NORC2017-10) for sharing their ship time. Thanks to Haijiao Liu, Chao Wu, and Congcong Guo for their assistance during the sampling and sample determination. We would also like to thank Dongxiao Wang at the South China Sea Institute of Oceanology of the Chinese Academy of Sciences for providing CTD data, and the crews of R/V Shiyan 3 for their help with water sampling.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Maps of the study area and the distribution of sampling stations. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
Figure 1. Maps of the study area and the distribution of sampling stations. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
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Figure 2. Horizontal distribution(weight-average) of temperature and salinity (a,b) and vertical distribution of temperature and salinity (c,d). Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
Figure 2. Horizontal distribution(weight-average) of temperature and salinity (a,b) and vertical distribution of temperature and salinity (c,d). Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
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Figure 3. The vertical distribution of Nitrate (a), nitrite (b), ammonium (c), phosphate (d), silicate (e), and Chlorophyll a (f). Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
Figure 3. The vertical distribution of Nitrate (a), nitrite (b), ammonium (c), phosphate (d), silicate (e), and Chlorophyll a (f). Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB).
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Jmse 10 00628 g004a 550Jmse 10 00628 g004b 550
Figure 4. Distribution of pico in DIN and DIP. (a) Surfer (3 m, 25 m), (b) middle (50 m, 75 m, 100 m), and (c) bottom (150 m, 200 m). Distribution of pico in DSI and DIP. (d) Surfer (3 m, 25 m), (e) Middle (50 m, 75 m, 100 m), and (f) Bottom (150 m, 200 m). Distribution of pico in DSI and DIN. (g) Surfer (3 m, 25 m), (h) middle (50 m, 75 m, 100 m), and (i) bottom (150 m, 200 m). The dashed line indicates the Redfield ratio of N:P = 16:1, Si:P = 15:1, Si:N = 15:16. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB), Dissolved Inorganic Nitrogen (DIN), Dissolved Inorganic Phosphorus (DIP), Dissolved Silicate (DSI).
Figure 4. Distribution of pico in DIN and DIP. (a) Surfer (3 m, 25 m), (b) middle (50 m, 75 m, 100 m), and (c) bottom (150 m, 200 m). Distribution of pico in DSI and DIP. (d) Surfer (3 m, 25 m), (e) Middle (50 m, 75 m, 100 m), and (f) Bottom (150 m, 200 m). Distribution of pico in DSI and DIN. (g) Surfer (3 m, 25 m), (h) middle (50 m, 75 m, 100 m), and (i) bottom (150 m, 200 m). The dashed line indicates the Redfield ratio of N:P = 16:1, Si:P = 15:1, Si:N = 15:16. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB), Dissolved Inorganic Nitrogen (DIN), Dissolved Inorganic Phosphorus (DIP), Dissolved Silicate (DSI).
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Figure 5. The vertical distribution of pico. (a) Syn, (b) Pro and (c) PEuks. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB). Synechococcus (Syn), Prochlorococcus (Pro), and Picoeukaryotes (PEuks).
Figure 5. The vertical distribution of pico. (a) Syn, (b) Pro and (c) PEuks. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB). Synechococcus (Syn), Prochlorococcus (Pro), and Picoeukaryotes (PEuks).
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Figure 6. The vertical distribution of pico in three regions. (a) EQ, (b) BOB, and (c) EB. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB). Synechococcus (Syn), Prochlorococcus (Pro), Picoeukaryotes (PEuks).
Figure 6. The vertical distribution of pico in three regions. (a) EQ, (b) BOB, and (c) EB. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB). Synechococcus (Syn), Prochlorococcus (Pro), Picoeukaryotes (PEuks).
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Figure 7. Average cell abundance and percentage of pico. (a) Average cell abundance and percentage of every station. (b) Average cell abundance and percentage of different regions. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB). Prochlorococcus (Pro), Synechococcus (Syn), and Picoeukaryotes (PEuks).
Figure 7. Average cell abundance and percentage of pico. (a) Average cell abundance and percentage of every station. (b) Average cell abundance and percentage of different regions. Bay of Bengal (BOB), the Equator (EQ), and the eastern border of the Indian Ocean near Sumatra (EB). Prochlorococcus (Pro), Synechococcus (Syn), and Picoeukaryotes (PEuks).
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Figure 8. RDA (redundancy analysis) biplots between the response variables and explanatory variables. Synechococcus (Syn), Prochlorococcus (Pro), Picoeukaryotes (PEuks), Nitrate (NO3−), Nitrite (NO2−), Ammonium (NH4+), Phosphate (PO4-), Silicate (SIO32-), Depth (Dep), Temperature (Tem), Salinity (Sal), Chlorophyll a (Chl-a).
Figure 8. RDA (redundancy analysis) biplots between the response variables and explanatory variables. Synechococcus (Syn), Prochlorococcus (Pro), Picoeukaryotes (PEuks), Nitrate (NO3−), Nitrite (NO2−), Ammonium (NH4+), Phosphate (PO4-), Silicate (SIO32-), Depth (Dep), Temperature (Tem), Salinity (Sal), Chlorophyll a (Chl-a).
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Figure 9. Results of GAMs describing the abundance of pico variability with temperature, salinity, nitrate, and nitrite in the EIO. (a) the abundance of Syn with temperature. (b) the abundance of Syn with salinity. (c) the abundance of Syn with NO3−. (d) the abundance of Syn with NO2−. (e) the abundance of Pro with temperature. (f) the abundance of Pro with salinity. (g) the abundance of Pro with NO3−. (h) the abundance of Pro with NO2−. (i) the abundance of PEuks with temperature. (j) the abundance of PEuks with salinity. (k) the abundance of PEuks with NO3−. (l) the abundance of PEuks with NO2−. Solid blue lines represent smoothed mean relationships from GAMs, and shaded areas are 95% confidence intervals (R2 = 0.706). Prochlorococcus (Pro), Synechococcus (Syn), and Picoeukaryotes (PEuks), Nitrate (NO3−), Nitrite (NO2−).
Figure 9. Results of GAMs describing the abundance of pico variability with temperature, salinity, nitrate, and nitrite in the EIO. (a) the abundance of Syn with temperature. (b) the abundance of Syn with salinity. (c) the abundance of Syn with NO3−. (d) the abundance of Syn with NO2−. (e) the abundance of Pro with temperature. (f) the abundance of Pro with salinity. (g) the abundance of Pro with NO3−. (h) the abundance of Pro with NO2−. (i) the abundance of PEuks with temperature. (j) the abundance of PEuks with salinity. (k) the abundance of PEuks with NO3−. (l) the abundance of PEuks with NO2−. Solid blue lines represent smoothed mean relationships from GAMs, and shaded areas are 95% confidence intervals (R2 = 0.706). Prochlorococcus (Pro), Synechococcus (Syn), and Picoeukaryotes (PEuks), Nitrate (NO3−), Nitrite (NO2−).
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Figure 10. Comparison of the results between chlorophyll and the concentration and cell abundances of pico. (a) Synechococcus (Syn), (b) Prochlorococcus (Pro), (c) Picoeukaryotes (PEuks).
Figure 10. Comparison of the results between chlorophyll and the concentration and cell abundances of pico. (a) Synechococcus (Syn), (b) Prochlorococcus (Pro), (c) Picoeukaryotes (PEuks).
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Wang, X.; Wang, F.; Sun, J. Distribution and Environmental Impact Factors of Picophytoplankton in the Eastern Indian Ocean. J. Mar. Sci. Eng. 2022, 10, 628. https://doi.org/10.3390/jmse10050628

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Wang X, Wang F, Sun J. Distribution and Environmental Impact Factors of Picophytoplankton in the Eastern Indian Ocean. Journal of Marine Science and Engineering. 2022; 10(5):628. https://doi.org/10.3390/jmse10050628

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Wang, Xingzhou, Feng Wang, and Jun Sun. 2022. "Distribution and Environmental Impact Factors of Picophytoplankton in the Eastern Indian Ocean" Journal of Marine Science and Engineering 10, no. 5: 628. https://doi.org/10.3390/jmse10050628

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