Zooplankton abundance, biovolume and size spectra at western boundary currents in the subtropical North Pacific during winter 2012

Journal of Marine Systems 155 (2016) 73–83

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Zooplankton abundance, biovolume and size spectra at western boundary currents in the subtropical North Pacific during winter 2012 Luping Dai a,b, Chaolun Li a,⁎, Guang Yang a, Xiaoxia Sun c a b c

Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, China University of Chinese Academy of Sciences, 19 Yuquan Road, Beijing 100049, China Jiaozhou Bay Marine Ecosystem Research Station, Chinese Ecosystem Research Network, 7 Nanhai Road, Qingdao 266071, China

a r t i c l e

i n f o

Article history: Received 15 August 2015 Received in revised form 7 November 2015 Accepted 11 November 2015 Available online xxxx Keywords: Zooplankton Normalized biovolume size spectra ZooScan Epipelagic zone Western Pacific Western boundary currents

a b s t r a c t Horizontal changes in mesozooplankton abundance, biovolume and size spectra at western boundary currents in the subtropical North Pacific during winter 2012 were evaluated by ZooScan measurement on samples collected by net towing from 23 stations. Zooplankton abundance and biovolume ranged from 35.1 to 456.8 ind. m−3 and 4.3 to 231.7 mm3 m−3, respectively. Copepoda were the most dominant species, followed by Chaetognatha and Tunicata. According to the Bray–Curtis cluster analysis based on biovolume of zooplankton size classes of each taxonomic group at intervals of 1 (log2 mm3 ind.−1) between −6 and 12 and considering the effect of regional factors, zooplankton communities were classified into four groups, which basically coincided with the geographical patterns of different currents: the North Equatorial Current (NEC), the North Equatorial Counter Current (NECC), the Kuroshio Current (KC), and the Mindanao Eddy (ME), respectively. The largest and lowest biovolumes were observed in the NECC region and the NEC region, respectively, and both were dominated by the 0.3 to 1 mm equivalent spherical diameter (ESD) size class, while the ME region was dominant by the 1 to 2 mm ESD size class. The slopes of the normalized biovolume size spectra for each group were slightly lower than −1 (range from −0.85 to −0.92), which indicates that zooplankton communities in the study area were characterized by low productivity and high energy transfer efficiency. © 2015 Elsevier B.V. All rights reserved.

1. Introduction In aquatic ecosystems, zooplankton play a central role by linking the base of the pelagic food web to higher trophic levels (Banse, 1995; Wassmann et al., 2006). They also are of great importance in biogeochemical cycles, energy flow, and vertical particle flux (Buitenhuis et al., 2006; Kiørboe, 1998; Reynolds, 2001; Sanders and Wickham, 1993). In addition, the biological pump process is thought to be related to the size of dominant zooplankton (Ducklow and Steinberg, 2001; Michaels and Silver, 1988). Therefore, from the perspectives of both food web dynamics and the biological pump, it is important to study the characteristics of the zooplankton community, such as abundance, biovolume, and size spectra. The normalized biovolume size spectra (NBSS) have been widely used around the world to evaluate the size spectra of zooplankton communities (Matsuno et al., 2012; Platt and Denman, 1977, 1978; Sato et al., 2015; Trudnowska et al., 2014; Zhou et al., 2015). New technologies are being developed to qualify the size of zooplankton. The semi-automatic ZooScan system provides not only robust estimates of zooplankton biovolume but also important taxonomic information (Gorsky et al., ⁎ Corresponding author. Tel.:+ 86 532 82898599. E-mail addresses: [email protected] (L. Dai), [email protected] (C. Li).

http://dx.doi.org/10.1016/j.jmarsys.2015.11.004 0924-7963/© 2015 Elsevier B.V. All rights reserved.

2010; Grosjean et al., 2004; Schultes and Lopes, 2009). In recent years, the size spectra evaluated by NBSS through the ZooScan system have been widely used to analyze biological properties in marine ecosystems (Forest et al., 2012; García-Comas et al., 2014; Lebourges-Dhaussy et al., 2014; Marcolin et al., 2013; Ohman et al., 2012; Schultes et al., 2013; Vandromme et al., 2014). The parameters of the NBSS represent the inherent properties of zooplankton communities or marine ecosystems: a steeper slope of the NBSS indicates high productivity and low energy transfer efficiencies in marine ecosystems (Sprules and Munawar, 1986; Zhou, 2006); higher intercept values reflect higher primary production of a community (Marcolin et al., 2013; Zhou, 2006). Thus, analysis of the NBSS provides insight into the structure of marine ecosystems. Pacific western boundary currents (Pacific WBCs) impact the global ocean circulation and climate variability by exchanging mass, heat, and salinity between the subtropical and tropical oceans (Hu et al., 2015). In the Northern Hemisphere, Pacific WBCs include the Kuroshio Current (KC) and the Mindanao Current (MC). Both of them are branches of the North Equatorial Current (NEC): as the westward-flowing NEC arriving at the Philippine coast, the NEC bifurcates and feeds the northwardflowing KC (Stommel and Yoshida, 1972) and the southward-flowing MC (Gordon et al., 2014). Furthermore, the MC produces the eastwardflowing North Equatorial Counter Current (NECC) (Johnson et al., 2002). Due to the influence of the Pacific WBCs, the Western Pacific

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In the present study, zooplankton abundance, biovolume, and size spectra at WBCs in the subtropical North Pacific were evaluated using ZooScan measurements of zooplankton samples collected using conical plankton nets during winter 2012. Size spectra were used as an indicator to examine zooplankton responses to upwelling and currents. NBSS analyses were conducted and results were compared with reported NBSS data from various oceans. Spatial variability in the size spectra of zooplankton at WBCs in the subtropical North Pacific was also studied. 2. Materials and methods 2.1. Zooplankton sampling Twenty-three stations were sampled by the RV “KE XUE YI HAO” in the Western Pacific Ocean from November 26 to December 12, 2012 (Fig. 1, Table 1). Samples were collected from 0 to 200 m by vertical tows with a conical plankton net (mouth opening 0.2 m2, mesh size 160 μm). A Hydro-Bios flowmeter was mounted in the mouth of the net to estimate the volume of water filtered through the net. Zooplankton samples were preserved immediately in 5% buffered formalin–seawater solution. At each station, temperature and salinity were recorded using a SeaBird CTD (SBE 911 plus). Seawater used for the analysis of chlorophyll a (Chl a) concentration was collected from 5, 30, 50, 75, 100, 150, and 200 m depths. These samples were filtered through Whatman GF/F filters and extracted using 90% aqueous acetone, and fluorescence was measured using a Turner Trilogy device. 2.2. ZooScan analysis Fig. 1. Location of the sampling stations in the Western Pacific Ocean between November 26 and December 12, 2012. Approximate positions of the main currents are depicted: KC: Kuroshio Current, NEC: North Equatorial Current, MC: Mindanao Current, ME: Mindanao Eddy, and NECC: North Equatorial Countercurrent (cf. Hu et al., 2015).

The calculations of zooplankton abundance and individual biovolume were carried out using a semi-automatic ZooScan system (HYDROPTIC). In the laboratory, each preserved sample was split into 8–128 aliquots containing about 2000 objects with a Motoda box splitter (Motoda, 1959). Subsamples, usually between 1/2 and 1/16 of the original samples, were scanned in the scanning cell of a 15 cm × 24 cm area and digitized with 2400 dpi resolution. After processing the samples with ZooProcess, each detected object was automatically classified according to a learning set, and then corrections were made manually. By default, only objects having an equivalent spherical diameter (ESD) of N 300 μm were detected and processed (see Chang et al., 2012; Gorsky et al., 2010; Grosjean et al.,

Ocean is regarded as a center of origin, with high species diversity (Allen, 2008; Briggs, 2005; Tittensor et al., 2010). However, very little is known about the zooplankton community in the Pacific WBCs environment in the Northern Hemisphere, apart from previous studies that analyzed the community structure of micronekton (Hidaka et al., 2003) and the zooplankton community structure in the Philippine Sea (Dai et al., 2014).

Table 1 Comparison of zooplankton abundance, biovolume and NBSS (Y = a + bX) of the four groups in the Western Pacific Ocean between November 26 and December 12, 2012. Parameter

Group A (7)

Abundance (ind. m−3) Total 0.3 to 1 mm 1 to 2 mm 2 to 3 mm 3 to 4 mm 4 to 5 mm N5 mm Biovolume (mm3 m−3) Total 0.3 to 1 mm 1 to 2 mm 2 to 3 mm 3 to 4 mm 4 to 5 mm N5 mm NBSS Slope (b) Intercept (a)

B (4)

C1 (6)

One-way ANOVA

Fisher's PLSD

C2 (6)

58.7 ± 20.4 56.8 ± 19.9 1.7 ± 0.9 0.1 ± 0.1 0.01 ± 0.03 0.00 ± 0.01 0.00 ± 0.00

379.9 ± 34.7 365.4 ± 34.3 13.0 ± 2.4 1.2 ± 0.8 0.21 ± 0.06 0.00 ± 0.00 0.02 ± 0.03

187.0 ± 54.6 181.2 ± 54.3 5.0 ± 2.2 0.5 ± 0.4 0.16 ± 0.34 0.11 ± 0.16 0.01 ± 0.01

184.6 ± 48.2 176.7 ± 45.6 7.5 ± 3.0 0.4 ± 0.2 0.04 ± 0.10 0.00 ± 0.00 0.01 ± 0.01

** ** ** ** NS NS NS

B C1 C2 A B C1 C2 A B C2 C1 A B C1 C2 A

12.0 ± 4.6 4.9 ± 1.7 4.3 ± 2.3 1.8 ± 1.5 0.5 ± 1.4 0.4 ± 1.1 0.0 ± 0.0

126.1 ± 70.1 36.2 ± 2.9 34.1 ± 7.9 20.1 ± 13.2 9.4 ± 3.3 0.0 ± 0.0 26.3 ± 44.4

64.4 ± 57.2 16.3 ± 3.7 12.3 ± 6.0 8.3 ± 5.9 8.2 ± 17.8 9.5 ± 12.8 9.7 ± 20.4

47.9 ± 21.6 16.5 ± 4.6 19.8 ± 8.8 6.3 ± 3.2 1.9 ± 4.6 0.0 ± 0.0 3.5 ± 5.4

** ** ** ** NS NS NS

B C1 C2 A B C2 C1 A B C2 C1 A B C1 C2 A

−0.89 ± 0.09 0.36 ± 0.65

−0.92 ± 0.04 3.27 ± 0.18

−0.88 ± 0.13 2.07 ± 0.51

−0.85 ± 0.04 2.29 ± 0.39

NS **

B C2 C1 A

Values are mean ± standard deviation. Numbers in parentheses indicate the number of sampling stations belonging to each group. Differences between the groups were tested by one-way ANOVA and Fisher's PLSD. Any two zones not connected by underlines are significantly different (Fisher's PLSD, p b 0.05). **p b 0.01, NS: not significant.

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2004 for details). Zooplankton taxonomic groups were identified through the ZooScan system. 2.3. Zooplankton abundance and biovolume The abundance (ind. m−3) of total zooplankton or of each taxonomic group was calculated as follows: abundance = number of organisms with same taxonomic group ∗ splitting ratio / net volume. Zooplankton biovolume (mm3 m− 3) was calculated from the following equation: biovolume = volume of organisms with same taxonomic group ∗ splitting ratio / net volume. Zooplankton volume equal to the ellipsoidal volume derived from ZooScan. Ellipsoidal volume (mm3) was calculated as (4/3)π(Major / 2)(Minor / 2)2, where Major and Minor axes (mm) of each object were provided by ZooScan. 2.4. Cluster analysis Cluster analysis was performed to evaluate spatial variability in the size spectra of zooplankton. To prepare for analysis, the biovolume data for each taxonomic group were separated into 21 size classes between −8 and 12 at intervals of 1 based on log2 zooplankton volume (mm3 ind.− 1), that was − 8 to − 7, − 7 to − 6,…, 11 to 12 (log2 mm3 ind.− 1). Similarity matrices were evaluated using the Bray– Curtis method based on the biovolume data and the latitude (Bray and Curtis, 1957). To group the samples, the similarity indices were coupled with hierarchical agglomerative clustering using a complete linkage method (unweighted pair group method using the arithmetic mean, UPGMA; Field et al., 1982). All these analyses were carried out using PRIMER software. To clarify how environmental parameters (latitude, longitude, surface sea temperature and salinity, temperature and salinity at 200 m depth, integrated mean temperature and salinity at 0 to 200 m water column) related to the samples, Redundancy Analysis (RDA) was performed using CANOCO software. 2.5. Normalized biovolume size spectra (NBSS) According to the ZooScan data, the NBSS were calculated following Platt and Denman (1977): the X-axis [log2 zooplankton volume (mm3 ind.−1)] was calculated by dividing zooplankton biovolume (B, mm3 m− 3) by the abundance of each size class [(ind. m− 3)] and converting to log2; the Y-axis [log2 normalized biovolume (m−3)] was calculated by dividing B in each size class by the interval of each size class [Δvolume (mm3)] and converting to log2. Regression analysis was carried out using the least squares regression (Quinones et al.,

Fig. 2. The average NBSS of the 23 zooplankton sampling stations in the Western Pacific Ocean between November 26 and December 12, 2012. Symbols indicate the mean for each size class; white symbols indicate size classes smaller than the mode used in this study.

Fig. 3. Horizontal distribution of zooplankton abundance (a) and biovolume (b) in the Western Pacific Ocean between November 26 and December 12, 2012.

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2003), then an NBSS linear model was calculated: Y = a + bX, where a and b are the intercept and the slope of the NBSS, respectively. When creating the NBSS, smaller organisms may be underestimated because of the mesh size (Fig. 2). To avoid that, we determined the

smallest size class under the approach of García-Comas et al. (2014), and chose the size class with maximum biovolume in the 23 samples as the smallest size class. The largest size class contained the largest organisms. Finally, a maximum of 19 size classes were contained in the

Fig. 4. Results of cluster analysis based on zooplankton biovolume size spectra. (a) Groups were identified by Bray–Curtis similarity in conjunction with UPGMA. (b) RDA plots of each group. The environmental parameters are indicated by arrows: latitude (Lat), longitude (Lon), surface sea temperature (ST) and salinity (SS), temperature (BT) and salinity (BS) at 200 m depth, integrated mean temperature (AT) and salinity (AS) at 0 to 200 m water column. (c) Distribution of the clustering results.

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NBSS. The minimum limit of the size classes was −6 (log2 mm3 ind.−1), corresponding to the volume of a 310 μm ESD sphere. The maximum limit was 12 (log2 mm3 ind.−1) or 19,851 μm ESD. The zero values of B were treated as empty size classes in the NBSS, because they were eliminated during the log transformation. 2.6. Statistical analysis According to the zooplankton sample groups clustered based on their size spectra, inter-group differences in hydrography (surface sea temperature and salinity, temperature and salinity at 200 m depth, integrated mean temperature and salinity at 0 to 200 m water column) and zooplankton data (abundance, biomass, and slope of the NBSS) were compared using one-way analysis of variance (ANOVA) and Fisher's protected least-squares difference (PLSD) method. To identify the factors that influenced the slope of the NBSS, an analysis of covariance (ANCOVA) was conducted using SPSS software, with zooplankton group as independent variable, the intercept of the NBSS as covariate and the slope of NBSS as dependent variable. 3. Results 3.1. Hydrography Sea surface temperature ranged from 24.8 to 29.8 °C and exhibited a tendency to increase from the northern stations to the southern stations. Temperature decreased with depth, and the temperature at 200 m depth ranged from 10.8 to 20.7 °C. The integrated mean temperature of the 0 to 200 m water column at each station varied from 21.5 to 26.5 °C. Sea surface salinity ranged from 33.1 to 34.5 and showed a pattern opposite to that of sea surface temperature and thus was lower in the southern stations and higher in the northern stations. The salinity at 200 m depth and the integrated mean salinity varied from 34.3 to 35.2 and from 34.4 to 34.9, respectively. 3.2. Zooplankton abundance, biovolume Zooplankton abundance ranged from 35.1 to 456.8 ind. m−3 (mean 206.6 ± 128.6) (Fig. 3a). In general, abundance increased from the coastal zone to the pelagic area and decreased from 3°N to 13°N along 130°E. Zooplankton biovolume ranged from 4.3 to 231.7 mm3 m− 3

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(mean 55.2 ± 55.5) (Fig. 3b). Its distribution pattern was similar to that of abundance, except for the reduction in biovolume from the coast to the offshore area along 18°N. Thirteen diverse zooplankton taxonomic groups were occurred: Amphipoda, Chaetognatha, Copepoda, Euphausiacea, Fish larva, Gastropoda, Luciferida, Medusa, Nauplius larva, Ostracoda, Polychaeta, Tunicata and Other zooplankton in this study. Among the 13 taxonomic groups, the numerically dominant zooplankton groups were Copepoda (83.6%) followed by Tunicata (4.2%) and Chaetognatha (3.8%). Gelatinous zooplankton are generally considered to include Medusa, Tunicata and Chaetognatha (Alldredge, 1984), and here it accounted for 9.2% of the total abundance. For biovolume, Copepoda accounted for 34.3% of the total biovolume, followed by Tunicata (15.3%) and Chaetognatha (14.0%), which was different from the proportion based on abundance.

3.3. Zooplankton community Based on the biovolume data for the size classes of each taxonomic group at intervals of 1 (log2 mm3 ind.−1) and the latitude, zooplankton communities were classified into two groups (Fig. 4a). Group A included sampling stations located at the 18°N transect and the northern part of the 130°E transect. The other group contained two subgroups, with subgroup B stations at the southern part of the 130°E transect and subgroup C stations at the 23°N transect and the middle part of the 130°E transect. According to the dendrogram (Fig. 4a), subgroup C was divided into C1 and C2, which included the 23°N transect sampling stations and the middle part of the 130°E transect, respectively. Ultimately, zooplankton communities were classified into four groups in this study: group A, group B, group C1, and group C2 (Fig. 4c). Fig. 4b shows the effects of hydrographic variables on these groups. Vertical profiles of temperature, salinity and chlorophyll a are shown in Fig. 5. The water mass structure in group C1 was characterized by the lowest sea surface temperature and the highest sea surface salinity. Below 100 m depth, the water mass of group A was characterized by salinity between 34.9 and 35.1 and was identified as North Pacific Tropical Water (NPTW). The water mass in group B had salinity higher than 35.2, which belonged to the South Pacific Tropical Water (SPTW). The highest concentrations of Chl a was also observed in group B. There was cold water upwelling at 200 m depth in group C2, and the salinity was lower than that of the NPTW and SPTW (Fig. 5).

Fig. 5. Vertical distribution of temperature, salinity and chlorophyll a of the four groups in the Western Pacific Ocean between November 26 and December 12, 2012. Temperature and salinity data were based on the values at 1 m intervals from CTD profiles.

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Total abundance significantly varied based on groups: it was highest for group B, followed by group C1 and group C2, and it was lowest for group A (Table 1). Total abundance was due to the dominance of the 0.3 to 1 mm ESD size class for all groups. For the 1 to 2 mm and 2 to 3 mm ESD size classes, the highest and the lowest abundances were also observed in groups B and A, respectively. The 4 to 5 mm ESD size class was most abundant in group C1. As for the taxonomic composition of each group, Copepoda were especially abundant in all four groups and completely dominated the community (Fig. 6a). Group A had the highest proportion of Copepoda (as high as 88.4%). The contribution of gelatinous zooplankton was highest for group B and accounted for 11.7% of total abundance. Group C1 was characterized by the appearance of a few Luciferida.

Total biovolume exhibited a pattern similar to that of total abundance (Table 1, Fig. 6c). The highest biovolume was observed for group B, due to the 0.3 to 1 mm ESD size class dominated by Copepoda (Fig. 7). The lowest biovolume occurred for group A, which lacked the N 5 mm ESD size class. Within the size class, group C1 contained the highest biovolume of the 4 to 5 mm ESD size class attributed to gelatinous zooplankton, whereas group B had the highest biovolume of the other size classes (0.3 to 1 mm, 1 to 2 mm, 2 to 3 mm, 3 to 4 mm, N5 mm). Group C2 was dominated by the 1 to 2 mm ESD size class, which was different from the other groups. The composition of zooplankton taxonomic groups in each size class differed by group (Fig. 7). Copepoda dominated mainly in the 0.3 to 1 mm and 1 to 2 mm ESD size classes, while gelatinous zooplankton were more dominant in the larger size classes. For the taxonomic composition of each group, the proportion of Copepoda decreased while that of gelatinous zooplankton increased, which was different from that based on abundance (Fig. 6b). 3.4. NBSS Fig. 8 shows the mean NBSS for each group. All NBSS were linear, although a slight “dome” was observed for group C1. This “dome” occurred on the X-axis at approximately 5–6, which corresponds to the 4 to 5 mm ESD size class containing the gelatinous zooplankton and Euphausiacea (Fig. 7). The slope of the NBSS for each group ranged from − 0.85 to − 0.92, and no significant inter-group differences were observed (Table 1). The intercept of the NBSS was highest for group B and lowest for group A. The intercept of group C2 was slightly higher than that of group C1. According to the ANCOVA analysis, there was no interaction between group and intercept (Table 2), but significant relationships were found between the slope and both the intercept (p b 0.01) and the group (p b 0.05) (Table 2). Moreover, all of the mean NBSS lacked or were low in larger size classes (N 7 (log2 mm3 ind.−1) or 2902 μm ESD), which may be due to the underestimation of larger organisms caused by the mesh size (Fig. 7). 4. Discussion 4.1. Zooplankton abundance, biovolume and taxonomic composition

Fig. 6. Zooplankton composition of the four groups in the Western Pacific Ocean between November 26 and December 12, 2012. (a) Taxonomic composition of each group based on mean abundance. Boxes filling with white dots indicate the gelatinous zooplankton. (b) Taxonomic composition of each group based on mean biovolume. (c) Mean biovolume and size composition (ESD, mm) of each group.

The abundance and biovolume of zooplankton at WBCs in the subtropical North Pacific were calculated in this study. The values (35.1 to 456.8 ind. m−3 and 4.3 to 231.7 mm3 m−3, respectively) were in the range of the reported abundance (16.8 to 1076 ind. m− 3) and biovolume (2.24 to 1007 mm3 m− 3) in the Northwest Pacific Ocean (Sato et al., 2015), but the mean abundance (206.6 ± 128.6 ind. m−3) was lower than that of the East China Sea (1049 ± 1882 ind. m− 3 (García-Comas, et al., 2014)). The abundance of zooplankton was also lower than that in the subarctic, transitional, and subtropical regions in the North Pacific (431, 226, and 278 ind. m−3, respectively, as reported by Matsuno and Yamaguchi (2010) and 401, 299, and 379 ind. m−3, respectively, as reported by Fukuda et al. (2012)). For the taxonomic composition of zooplankton at WBCs in the subtropical North Pacific, Copepoda were the most abundant and accounted for a fairly large proportion of the total zooplankton (as high as 83.6%) (Fig. 6a), which fully reflected their dominant position in this oceanic ecosystem. Moreover, Copepoda accounted for 34.3% to the total biovolume. Our result was in the range reported for Copepoda of the equatorial Pacific at 175°E (30–71%) (Ishizaka et al., 1997). We also found that Tunicata ranked second in terms of the attribution to total biovolume, whereas Ishizaka et al. (1997) reported that Chaetognatha ranked second. This may be because the biomass in our study was based on biovolume whereas that in Ishizaka's study was based on carbon biomass. This type of discrepancies caused by quantitative methods was also observed in taxonomic composition. Copepoda, Tunicata and Chaetognatha were the top three dominant taxonomic

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Fig. 7. Biovolume composition of zooplankton taxonomic groups in each size class for the four groups in the Western Pacific Ocean between November 26 and December 12, 2012. Boxes filling with white dots indicate the gelatinous zooplankton.

groups at WBCs in the subtropical North Pacific both based on abundance and biovolume. These three groups covered totally 91.6% for abundance, while only composed 63.6% for biovolume. Also, for taxonomic composition of each group, the proportion of Copepoda based on abundance was higher than that based on biovolume while it was contrary for gelatinous zooplankton (Fig. 6a and b). Abundance was an important quantitative index in zooplankton study. However, individual body size was different between taxonomic groups, as well as life stages of one species. So abundance cannot fully reflect how much zooplankton occurred. Biovolume was another quantitative index to show distribution patterns of zooplankton. It was based on individual volume regardless of water content and biochemical components which differed in different taxonomic groups. Thus, it is of great importance that abundance and biovolume should be combined to assess the zooplankton community. Gelatinous zooplankton were especially abundant in group B compared with other groups and accounted for as high as 11.7% of total abundance (Fig. 6a). Since gelatinous zooplankton species are generally recognized as predators that mostly feed on microzooplankton, mesozooplankton and fish larvae, they have important impacts on the pelagic food web dynamics (Colin et al., 2005). Temperature is considered to be one of the most important factors influencing the distribution of gelatinous zooplankton (Buecher and Gibbons, 2000; Gili et al., 1987), and more gelatinous zooplankton assemblages have been reported in warmer waters (Pagès and Gili, 1991; Pavez et al., 2010). In the current study, gelatinous zooplankton were more abundant in group B where the sea surface temperature was high. It has also been reported that the presence of upwelling may affect the abundance and horizontal

distribution of gelatinous zooplankton (Pavez et al., 2010). Higher densities of hydromedusae were detected during the upwelling season in the Tropical East Pacific (Miglietta et al., 2008). In tropical oceans, the generally stable temperature and light conditions allow plankton communities to respond quickly to nutrient enhancement (López-López et al., 2013). The upwelling in the group B area increased the vertical mixing of the water column and enhanced nutrient concentrations in the upper water. Gelatinous zooplankton respond to the increased productivity through the food chain. Accordingly, a high abundance of gelatinous zooplankton was found in this area. Luciferida were only observed in group C1 which was mainly affected by KC. A single genus, Lucifer, belongs to the family Luciferidae (Burkenroad, 1981, 1983). One of the seven species of Lucifer is Atlantic species, while the others occur in the Western Pacific (Hashizume and Omori, 1998). Based on salinity adaptations, Lucifer species can be sorted into off-shore species with an optimal salinity from 32 to 34 and oceanic species with an optimal salinity over 34 (Xu, 2010). The Luciferida found in group C1 were oceanic species because the salinity in this area was higher than 34. In the Northwestern Pacific, Lucifer typus was reported to be an oceanic species that is mainly distributed in waters influenced by KC (Hashizume and Omori, 1998; Omori, 1977). 4.2. Spatial variability Based on the above mentioned results, the horizontal distributions of each zooplankton group in this study showed distinct geographical patterns that were coupled with the different currents (Fig. 4c). According to the patterns of the Pacific WBCs (Hu et al., 2015), groups A, B, C1

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Fig. 8. Mean NBSS of four groups in the Western Pacific Ocean between November 26 and December 12, 2012.

and C2 were mainly influenced by the NEC, NECC, KC and ME, respectively (Fig. 4c). Group B was observed in the southernmost areas of our survey region and covered sample stations 3° to 6°N along the 130°E transect, which was located in the NECC affected area. It was characterized by the highest zooplankton abundance and biovolume among the four groups in this study. A similar pattern was reported in the central Pacific and eastern Pacific (King and Demond, 1953; Reid, 1962; White et al., 1995). According to the NORPAC survey, zooplankton volume in the NECC was higher than that in the NEC in tropical and subtropical waters (Reid, 1962). King and Demond (1953) found the highest zooplankton volumes at the north edge of the NECC in their investigation of zooplankton abundance in the central Pacific. In the equatorial Pacific at 140°W, the zooplankton biomass maximum was observed several degrees to the north and south of the equator (White et al., 1995). The high values of zooplankton abundance and biovolume in the NECC are determined by both upwelling and primary production. The equatorial Pacific is characterized by high nitrate and low chlorophyll conditions. The upwelling in the NECC brings high nutrient sub-surface water to the euphotic layer at the equator divergence, and phytoplankton develop rapidly in the fresh rising water and produce high concentrations of Chl a (Sun, unpublished data). Zooplankton respond to the enhanced food abundance via the bottom-up effect and generate high biovolume (Dessier and RenéDonguy, 1985; Fiedler et al., 1992; Vinogradov and Shushkina, 1989). Moreover, variations of phytoplankton production affect zooplankton biomass in the equatorial Pacific (Dessier and RenéDonguy, 1985; Vinogradov, 1981; Vinogradov and Shushkina, 1989). A positive correlation between zooplankton grazing and primary production has been reported (Roman et al., 1995; Zhang et al., 1995). Synchronous observations of primary production indicated high values

in the NECC (Sun, unpublished data), which provide the food necessary for the growth and reproduction of zooplankton. These factors explain the high zooplankton abundance and biovolume in NECC affected areas. Group A was observed in regions of the 18°N transect and the north part of 11°N along the 130°E transect, which was mainly influenced by the NEC. Group A was characterized by the lowest zooplankton abundance and biovolume. The Chl a concentration and primary production in the group A area remained at a low level according to the Synchronous observation data (Sun, unpublished data). On the one hand, zooplankton grazing limits the growth of phytoplankton; on the other hand, the ammonium excreted by the zooplankton provides nitrogen nutrients for phytoplankton growth and supports primary production. Table 2 Result of the ANCOVA for the slope (b) of the NBSS (Y = a + bX). Custom model Source of variation

df

Mean square

F-value

p-value

Intercept Group Group × intercept Error

1 3 3 15

0.021 0.014 0.005 0.006

3.523 2.308 0.849 –

NS NS NS –

With the interaction term removed Source of variation

df

Mean square

F-value

p-value

Intercept Group Error

1 3 18

0.053 0.019 0.006

8.970 3.268 –

** * –

With zooplankton group (cf. Fig. 5c) applied as independent variables and the intercept (a) of the NBSS applied as covariate. df: degree of freedom, NS: not significant, **p b 0.01, *p b 0.05.

L. Dai et al. / Journal of Marine Systems 155 (2016) 73–83

In this circumstance, a dynamic equilibrium is reached (Syrett, 1981; Wheeler and Kokkinakis, 1990). Thus, the abundance and biovolume of zooplankton were low in this group under the condition of low Chl a and primary production. The abundance and biovolume of group C1 and group C2 were moderate in this study. Group C1 was present to the east of Taiwan and in the area influenced by the KC. Several studies reported that zooplankton biomass of the Kuroshio region was similar to or higher than that of the Japan Sea (Hirota and Hasegawa, 1999; Iguchi, 2004). However, zooplankton biovolume of the KC region in our study was lower than that in the Japan Sea (135.1 ± 34.1 mm3 m−3, Sato et al., 2015) and higher than that in the Kuroshio extension (10.7 ± 7.5 mm3 m−3, Sato et al., 2015). Group C2 was present at stations around 8°N along the 130°E transect and was mainly affected by the ME. Both the abundance and biovolume of these two groups were lower than those of group A, which may be due to transport by ocean currents. When the westward-flowing NEC arrives at the Philippine coast, the water carried by the NEC mixed with the nutrient-rich coastal water. The NEC then bifurcates and feeds the northward-flowing KC (Stommel and Yoshida, 1972) and the southward-flowing MC (Gordon et al., 2014). Thus, the water carried by KC and MC was richer in nutrient than that in NEC. The KC and MC waters supported the development of more phytoplankton (Sun, unpublished data), which provided food for zooplankton and resulted in higher zooplankton abundance and biovolume compared to those in the NEC. From the aspect of size class composition, group A also differed from group C1 and group C2. The distribution of 0.3 to 1 mm ESD size class was highest in group A (Fig. 6c), and small-sized Copepoda constituted 79.7% of this size class. A previous study showed that the body size of copepods is inversely correlated with habitat temperature (Corkett and McLaren, 1978). The highest integrated mean temperature at 0 to 200 m water column associated with group A may have allowed the development of small-sized Copepoda and led to the dominance of 0.3 to 1 mm ESD size class. However, compared with group A, group C2 was dominated by the 1 to 2 mm ESD size class, which was also consisted mainly by Copepoda. This may be due to the development of largersized Copepoda in the cold water upwelling in group C2. The hydrography of group C1 was marked and had the lowest sea surface temperature. As a result, the proportion of the 4 to 5 mm ESD size class in group C1 was higher than that in the other groups, which was similar to the scenario reported for the Japan Sea (Sato et al., 2015). This size range was composed mainly of macrozooplankton such as Tunicata, Medusae and

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Euphausiids. In general, size classes in group C1 and group C2 were larger than those in group A, which was caused by ocean current transport and temperature. This shows that physical processes can indirectly regulate the zooplankton community. 4.3. NBSS The NBSS have been used to evaluate the structure of marine ecosystems around the world (Matsuno et al., 2012; Quinones et al., 2003; Sato et al., 2015; Zhou et al., 2009). The slope of the NBSS is an index of productivity and transfer efficiency in each marine ecosystem (Sprules and Munawar, 1986; Zhou, 2006). According to Sheldon et al.'s (1972) results, in a stable marine system, the slope of the NBSS is approximately equal to − 1. Slopes steeper than that indicate higher productivity and lower transfer efficiency, whereas flatter slopes may emerge in a marine ecosystem with lower productivity and higher transfer efficiency (Rodriguez and Mullin, 1986; Sprules and Munawar, 1986). In our study, the NBSS slopes for each group were slightly lower than − 1 (Table 1). Thus, zooplankton communities at WBCs in the subtropical North Pacific are characterized by low productivity with high energy transfer efficiency. The intercept of the NBSS reflects the primary production of a community (Marcolin et al., 2013; Zhou, 2006). In this study, intercepts for each group were of the same order as simultaneously observed primary production (Sun, unpublished data). Some of the reported NBSS slopes worldwide are listed in Table 3. The NBSS slopes from this study were more moderate than those in the North Pacific Ocean and Northwest Pacific Ocean. The slope of group B was the most negative among the four groups and was similar to that of the Western Antarctic Peninsula in the fall, and this situation is considered to be in a natural balance (Zhou et al., 2009). The slopes of groups A, C1 and C2 were similar to the slope values from disturbed inshore regions, such as the Gulf of St. Lawrence (estuary) (Herman and Harvey, 2006), the East China Sea (García-Comas et al., 2014), and the South China Sea (Zhou et al., 2015). It has been reported that the slopes of the NBSS can be influenced by both bottom-up and top-down effects. Bottom-up processes such as increased nutrients bring about increased productivity and zooplankton abundance in smaller size classes and then produce steeper slopes, while top-down processes such as predation by zooplanktivorous species that selectively feed on zooplankton in larger size classes also lead to steeper slopes (Moore and Suthers, 2006). Thus, the steepest slope of the NBSS in group B may be due to the high abundance of smaller size classes (Table 1) caused by the

Table 3 Comparison of the slope (b) of NBSS (Y = a + b X) on the zooplankton community at various locations. Location/region

Unit

Size range (mm)

Slope

Measurements

References

Gulf of St. Lawrence (open water)

Biovolume

0.25 to 2

−0.47

Herman and Harvey (2006)

Barents Sea Tasman Sea South China Sea East China Sea Brazilian Continental Shelf (oceanic stations) Gulf of St. Lawrence (estuary) Western Antarctic Peninsula (fall) Chukchi Sea Coral Sea Northwest Pacific Ocean North Pacific Ocean Northwest Atlantic Ocean California Current Western Antarctic Peninsula (summer) California Bight

Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Biovolume Carbon Carbon Carbon Biovolume Biovolume

0.25 to 14 0.11 to 3.3 0.16 to 4 0.57 to 15 0.25 to 8 0.25 to 2 0.25 to 14 0.25 to 5 0.11 to 3.3 0.5 to 5 0.18 to 4.0 0.07 to 8.0 0.2 to 3.3 0.25 to 14 0.05 to 8.0

−0.63 (−0.44 to −0.91) −0.69 (−0.59 to −0.78) −0.82 (−0.67 to −0.93) −0.83 (−0.73 to −0.97) −0.91 (−0.61 to −1.41) −0.90 −0.92 −0.94 (−0.78 to −1.11) −0.97 (−0.94 to −0.99) −1.13 (−0.9 to −1.24) −1.13 (−0.77 to −1.48) −1.14 (−1.09 to −1.17) −1.43 (−0.53 to −1.96) −1.8 −2.3

Western Pacific (group A) Western Pacific (group B) Western Pacific (group C1) Western Pacific (group C2)

Biovolume Biovolume Biovolume Biovolume

0.31 to 20 0.31 to 20 0.31 to 20 0.31 to 20

−0.89 (−0.76 to −1.05) −0.92 (−0.88 to −0.99) −0.88 (−0.67 to −1.05) −0.85 (−0.82 to −0.91)

Laser optical plankton counter (LOPC) LOPC Optical plankton counter (OPC) Manual measurements ZooScan ZooScan LOPC OPC OPC OPC OPC Manual measurements Image analyzer OPC OPC Multi-frequency acoustic profiling system (MAPS) ZooScan ZooScan ZooScan ZooScan

Basedow et al. (2010) Baird et al. (2008) Zhou et al. (2015) García-Comas et al. (2014) Marcolin et al. (2013) Herman and Harvey (2006) Zhou et al. (2009) Matsuno et al. (2012) Baird et al. (2008) Sato et al. (2015) Rodriguez and Mullin (1986) Quinones et al. (2003) Huntley et al. (1995) Zhou et al. (2009) Napp et al. (1993) This study This study This study This study

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increased productivity induced by bottom-up effect, while the flattest slope of the NBSS in group C2 may be due to the increased abundance of larger size classes, just as the observed high value in the 1 to 2 mm ESD size class dominated by Copepoda and Chaetognatha (Fig. 7). 5. Conclusions Zooplankton communities at WBCs in the subtropical North Pacific were separated into four groups using ZooScan analysis of zooplankton samples. The horizontal distributions of each zooplankton group were coupled with the geographical patterns of different currents. All groups had NBSS slopes that were slightly lower than the theoretical value (−1). These results indicate that the zooplankton communities were characterized by low productivity with high energy transfer efficiency at WBCs in the subtropical North Pacific during winter in 2012. However, temporal variability of zooplankton communities and the ecological distribution of zooplankton in the mesopelagic and bathypelagic zone of the deep ocean in this region are still poorly known, and further studies of zooplankton in this region should be conducted. Acknowledgments This research was supported by “the Strategic Priority Research Program of the Chinese Academy of Sciences — Grant No. XDA11030200”, “Project jointly supported by Shandong Province and the NSFC — Grant No. U1406403” and “Project of Global Change and Air-Sea interaction — Grant No. GASI-02-PAC-ST-Wsum”. We thank the National Natural Science Foundation of China for providing the opening and sharing voyage during November to December 2012. We are grateful to the captain and crew of R.V. “KE XUE YI HAO” for their technical and logistical support. We greatly thank Peng Ji and Wuchang Zhang for their invaluable assistance during shipboard research activities. Thanks to Dongliang Yuan and Xiaoxia Sun for providing environmental parameters and to Mingliang Zhu for helping with the ZooScan data analyses. References Alldredge, A., 1984. The quantitative significance of gelatinous zooplankton as pelagic consumers. In: Fasham, M.J.R. (Ed.), Flows of Energy and Materials in Marine Ecosystems. Springer, US, pp. 407–433. Allen, G.R., 2008. Conservation hotspots of biodiversity and endemism for Indo–Pacific coral reef fishes. Aquat. Conserv. Mar. Freshw. Ecosyst. 18, 541–556. Banse, K., 1995. Zooplankton: pivotal role in the control of ocean production. ICES J. Mar. Sci. 52, 265–277. Basedow, S.L., Tande, K.S., Zhou, M., 2010. Biovolume spectrum theories applied: spatial patterns of trophic levels within a mesozooplankton community at the polar front. J. Plankton Res. 32, 1105–1119. Bray, J.R., Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27, 326–349. Briggs, J.C., 2005. The marine East Indies: diversity and speciation. J. Biogeogr. 32, 1517–1522. Buecher, E., Gibbons, M.J., 2000. Interannual variation in the composition of the assemblages of medusae and ctenophores in St. Helena Bay, Southern Benguela Ecosystem. Sci. Mar. 64, 123–134. Buitenhuis, E., Quéré, C.L., Aumont, O., Beaugrand, G., Bunker, A., Hirst, A., Ikeda, T., O'Brien, T., Piontkovski, S., Straile, D., 2006. Biogeochemical fluxes through mesozooplankton. Glob. Biogeochem. Cycles 20, GB2003. Burkenroad, M.D., 1981. The Higher Taxonomy and Evolution of Decapoda (Crustacea). San Diego Society of Natural History. Burkenroad, M., 1983. Natural classification of Dendrobranchiata, with a key to recent genera. Crustacean 279–290. Chang, C.-Y., Ho, P.-C., Sastri, A.R., Lee, Y.-C., Gong, G.-C., Hsieh, C.-h., 2012. Methods of training set construction: towards improving performance for automated mesozooplankton image classification systems. Cont. Shelf Res. 36, 19–28. Colin, S., Costello, J.H., Graham, W.M., Higgins III, J., 2005. Omnivory by the Small Cosmopolitan Hydromedusa Aglaura hemistoma. Corkett, C.J., McLaren, I.A., 1978. The biology of pseudocalanus. Adv. Mar. Biol. 15, 1–231. Dai, L., Li, C., Sun, X., Ji, P., Zhang, W., 2014. Abundance and biomass of zooplankton in Philippine Sea in winter 2012. Oceanol. Limnol. Sin. 1225–1233. Dessier, A., RenéDonguy, J., 1985. Planktonic copepods and environmental properties of the eastern equatorial Pacific: seasonal and spatial variations. Deep-Sea Res. Part A 32, 1117–1133.

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