Appendicularians in the southwestern Sea of Japan during the summer: abundance and role as secondary producers

Appendicularians in the southwestern Sea of Japan during the summer: abundance and role as... Abstract Appendicularian abundance was investigated at a total of 235 stations over 5 years, from 2011 to 2015, in southwestern Sea of Japan to evaluate potential factors influencing abundance and to understand their effects on the marine ecosystem. Oikopleura longicauda was the dominant appendicularian species, present in 232 samples, and with the highest abundance (mean ± SD: 463 ± 694 individuals m−3) among the appendicularians. Warm conditions appear to favour O. longicauda based on a generalized linear model, and salinity and chlorophyll a concentration were not significantly related to abundance. The abundance of O. longicauda was correlated significantly with those of Microsetella and Oncaea, which are the grazers of discarded appendicularian houses, as well as that of carnivorous Sagitta. Oikopleura longicauda houses, discarded daily to the water column, were estimated to represent a carbon flux of 7.7 ± 7.8 mg C m−2 d−1 (mean ± SD), depending on their density and water temperature. We estimate that a minimum of approximately 13% of houses were consumed by Oncaea and Microsettela. Therefore, we suggest that secondary production by O. longicauda in the southwestern Sea of Japan increased during summer and leads to enriched production at higher trophic levels in the epipelagic ecosystem during this season. INTRODUCTION Appendicularians, or larvaceans (Tunicata: Appendicularia), are cosmopolitan secondary producers and are the second most dominant zooplankton group in the world’s oceans. They are found, irrespective of warm or cold temperatures, in coastal zones and the open ocean, in eutrophic or oligotrophic waters (López-Urrutia et al., 2003; Steinberg et al., 2008; Jaspers et al., 2009). They are filter feeders and use a specialized outer casing or “house”, made by secreting mucus and cellulose, to filter and concentrate small food particles (Alldredge, 1976b). Once it becomes clogged with uneaten food particles and waste, the house is shed and a new house is secreted (Alldredge, 1976b). This feeding strategy is generally considered advantageous in oligotrophic oceans (López-Urrutia et al., 2003). Appendicularians discard 2–40 houses day−1, taking <5 min to rebuild a new house (Sato et al., 2001, 2003). Both appendicularians and their discarded houses play important roles in biological production and carbon cycling in oceans (Alldredge, 1972, 1976a; Robison et al., 2005). Appendicularian contribution to mesozooplankton secondary production increases with increasing productivity of the environment, and they are estimated to consume 8% of annual primary production in European coastal waters (López-Urrutia et al., 2003). Appendicularians are an important source of food for many fish species and zooplankton, such as the sergeant major, medusae, chaetognaths and ctenophores (Alldredge, 1976b). A large number of studies report that appendicularins are important food for carnivore medusae and various life stages of fish (Purcell et al., 2005). In Japanese coastal waters, larvae of flounders, Pleuronichthys cornutus, Pseudorhombus pentophthalmus and Paralichthys olivaceus, feed on appendicularians (Kuwahara and Suzuki, 1983; Ikewaki and Tanaka, 1993; Hasegawa et al., 2003). Larvae and juveniles of the Japanese sardine, Sardinops melanostictus, are also reported to be grazers of appendicularians (Watanabe and Saito, 1998), as are those of the red sea beam, Pagrus major (Shimamoto and Watanabe, 1994). A metagenetic study found that the larvae of the Pacific bluefin tuna, Thunnus orientalis, which spawns during the summer in southwestern Sea of Japan (Ohshimo et al., 2017), feed selectively on appendicularians (Kodama et al., 2017a). The discarded appendicularian houses, which sink rapidly through the water column, are an important component of marine snow (Hansen et al., 1996; Robison et al., 2005), and make a considerable input to carbon cycling in the oceans. Leptocephali of eight eel species feed selectively on appendicularian houses (Mochioka and Iwamizu, 1996). Both abandoned and occupied houses are an important source of food for pelagic copepods, such as Scolecithrix danae, Microsetella spp. and Oncaea spp., which are known to attach themselves to the houses prior to feeding on them (Ohtsuka and Kubo, 1991; Ohtsuka et al., 1993; Nishibe et al., 2015). The distribution and the abundance of appendicularians are usually related to temperature, salinity, food concentration and grazing pressure (Shiga, 1985; Taggart and Frank, 1987; Tomita et al., 2003; Shiganova, 2005; Hidaka, 2008; Lombard et al., 2010; Xu and Zhang, 2010). Regardless of species, increases in temperature in the optimal temperature range (~30°C) promote house renewal rates (Sato et al., 2001, 2003), enhance growth (López-Urrutia et al., 2003) and shorten appendicularian generation times (Sato et al., 2001; López-Urrutia et al., 2003; Lombard et al., 2009b; Deibel and Lowen, 2012). Increases in salinity decrease house renewal rates (Sato et al., 2001). Food concentration studies are limited to data on O. dioica and show that minimally constrained food concentrations (30 μg C L−1) restrict appendicularian body sizes (Touratier et al., 2003; Lombard et al., 2009a) and decrease growth rates (Troedsson et al., 2002). Growth rates adhere to a maximum upper limit under conditions of sufficient food (López-Urrutia et al., 2003; Lombard et al., 2009b; Deibel and Lowen, 2012). House renewal rates are also affected by food concentration (Fenaux, 1985; Selander and Tiselius, 2003; Tiselius et al., 2003); renewal rates only increase with concentration at low concentrations (Selander and Tiselius, 2003; Tiselius et al., 2003). Sato et al. (2001), however, showed that mean house renewal rates did not differ significantly under different food concentrations. Rather, food concentration significantly affected egg numbers (Troedsson et al., 2002; Nishida, 2008). Although temperature and availability of food may increase appendicularian abundance, these relationships are non-linear (Hidaka, 2008; Xu and Zhang, 2010). Moreover, Lombard et al. (2010) showed that appendicularian optimal food and temperature conditions are species-specific: O. longicauda is adapted to oligotrophic conditions; O. dioica prefers colder water than O. fusiformis and O. rufescens. In one of the few studies on predation pressure on appendicularians, Shiganova (2005) found that the abundance of Oikopleura dioica fell after invasion by a predator, the ctenophore Mnemiopsis leidyi, in the Black Sea. Appendicularians are one of the major zooplankton groups in the Sea of Japan, the semi-closed marginal sea in the western North Pacific (Tomita et al., 1999, 2003), and their abundance varies with the seasonal cycle of phytoplankton abundance in the Sea (Tomita et al., 2003). However, previous studies on appendicularians in the area were limited to Toyama Bay, where the summer phytoplankton bloom occurs due to river discharge (Terauchi et al., 2014). Additionally, the Changjiang discharged water, Kuroshio water and Taiwan Warm Current water are the sources of the Tsushima Warm Current, which flow in the southern part of the Sea of Japan (Senjyu et al., 2008). Therefore, the species composition and the abundance of appendicularians may be different horizontally with hydrographic and other environmental variables. Given that appendicularians are important prey items for fish and other organisms, an assessment of their abundance during summer is essential for understanding trophic relationships in the Sea of Japan. Therefore, we conducted surveys for 5 years to examine appendicularian abundance and species composition in the southwestern part of the Sea. We used a generalized linear model to evaluate environmental factors with potential to cause fluctuations in the abundance of appendicularians. We also considered the role of appendicularians as secondary producers in the Sea of Japan. METHODS Observations Oceanic observations were conducted in July, from 2011 to 2015, on board R/V Shunyo-Maru, Japan Fisheries Research and Education Agency (2011, 2014 and 2015), and R/V Shoyo-Maru, Fisheries Agency (2012 and 2013), at 49 stations (Stns 1–49) set every 10 or 15 nautical miles along five line transects (named A–E) in the southwestern Sea of Japan (Fig. 1). During the 2011 cruise, Stns 41–49 were not observed because of a shortage in ship time. Fig. 1. View largeDownload slide Map of sampling stations in the Sea of Japan. Open circles and numbers within them denote station positions and station numbers, respectively. Letters A–E denote different line transects. The grey shadow along the coast indicates the continental shelf. Fig. 1. View largeDownload slide Map of sampling stations in the Sea of Japan. Open circles and numbers within them denote station positions and station numbers, respectively. Letters A–E denote different line transects. The grey shadow along the coast indicates the continental shelf. At every station, vertical profiles of temperature and salinity were recorded using a conductivity–temperature–depth (CTD) sensor (SBE 9plus, Sea-Bird Scientific) with an in vivo chlorophyll (Chl) fluorescence sensor (ECO-AFL/FL, WET Labs, during the Shunyo-Maru cruises, and Chlorophyll Fluorometer, Seapoint, during the Shoyo-Maru cruises) and a carousel water sampling system (SBE 32, Sea-Bird Scientific) from ~5 to 500 m depth or 10 m above the bottom. Hydrographic data used in our study were obtained from depths <100 m because most of the appendicularians are present in the Sea of Japan at these depths (Tomita et al., 2003). At Stns 1 and 44, the depth of the sea bottom was <100 m; therefore, hydrographic data were obtained from depths shallower than this. For sea surface temperature (SST), seawater was sampled with a bucket and temperature measured with a calibrated mercury thermometer. Mixed layer depth (MLD) was determined based on the potential density criterion 0.125 (Levitus, 1982). Weekly mean sea surface height was derived from Ssalto/Duacs gridded absolute dynamic topography (www.aviso.altimetry.fr) for confirmation of mesoscale eddies. Water was sampled from the surface with a bucket at every station. The carousel water sampling system was used for discrete vertical sampling at odd numbered stations (20 stations in 2011 and 25 stations after 2012). For evaluating the vertical profile of Chl a concentration, water was collected at 11 depths above 200 m, particles in 300 mL of seawater were collected on a glass fibre filter (GF/F, Whatman), and the concentration was measured with a fluorometer (TD-700, Turner Designs, during the 2011–2013 cruises, and 10 AU during the 2014 and 2015 cruises) after extraction (Welschmeyer, 1994). For these data, in vivo Chl fluorescence was calibrated at every cruise regardless of time of day (r2 > 0.86). In vivo Chl fluorescence has a diel rhythm (Holm-Hansen et al., 2000); however, we ignored this because significant differences in diel slopes were observed only during the 2014 cruise (t-test, P = 0.03). Zooplankton were collected with vertical hauls of a long North Pacific standard plankton (Norpac) net (Nytal 13XX, 100 μm mesh, 0.45 m mouth diameter, Rigo) up to the surface from a depth of 200 m or from 10 m above the bottom. A flow metre (Rigo), calibrated after every cruise, was installed at the mouth of the net in order to estimate the volume of filtered water. Zooplankton samples were fixed with neutral formalin soon after sampling, and stored at room temperature until morphological identification. Individuals were identified to the lowest taxonomic level, and the abundance of each zooplankton species was calculated using counts of each species and water volume in each station (individuals per cubic metre, inds m−3). Statistical analyses The environmental factors affecting appendicularian abundances were evaluated with a generalized linear model (GLM), using the package “MASS” (Venables and Ripley, 2013) in R version 3.4.0 (R Core Team, 2017). We selected the best model based on the Bayesian information criterion (BIC); ΔBIC was calculated as the difference between the full model containing all covariates and the null model (intercept only) using “dredge” function in the “MuMin” package of R. The response variable was the common log-transformed abundance of each appendicularian species. The explanatory variables were SST, mean temperature from a depth of 10 to 100 m (water-column T), sea surface salinity (SSS), mean salinity from a depth of 10 to 100 m (water-column S), sea surface Chl a (SSChl a), mean Chl a from a depth of 10 to 100 m (water-column Chl a), MLD, haul depth (depth), year and time. Depth (shallow: <100 m; middle: 100–200 m; and deep: ≥200 m), year and time (divided twice-hourly) were categorical variables, while the other parameters were continuous variables and linked with linear functions. The continuous variables were standardized to 0 mean and 1 variance using the “vegan” package in R. We applied these analyses to the species which was present in ≥50% of the stations and whose abundance was normally or log-normally distribution. Normality of abundance data was tested with the Shapiro–Wilk test. We evaluated the environmental factors affecting appendicularian abundances with a generalized additive model (GAM) using the “mgcv” package; however, the BIC in the GLM was smaller than those of GAM, and the GLM was selected as the best-suited model. RESULTS Hydrography SST ranged 22–28°C in all sampling years (Fig. 2a). High SST values were observed across a wide area in 2014 (mean ± SD: 25.1 ± 0.8°C), while they were lower in 2013 and 2015 (23.4 ± 0.8°C in both years, Fig. 2a) than in 2014. In 2011, SSTs were higher in line B (Fig. 2a) than in other lines. Variations in water-column T (between 10 and 100 m depth) were different from those in SST (Fig. 2b). Water-column T was high (~15°C) near the coast of Honshu, for example at Stns 22 and 23, and low in the cyclonic eddies identified as low sea surface height (Fig. 2b). The high water-column T at Stns 1 and 44 reflected the shallow bottom at these stations. Yearly mean water-column T in the area was the highest in 2013 (18.0 ± 1.9°C) and the second highest in 2014 (17.4 ± 1.8°C). Generally, variations in mean water-column salinity at a depth of 10–100 m (water-column S) corresponded to variations in water-column T (Fig. 2c); salinity was low at stations where water-column T was low except in the coastal areas. Water-column S was higher (by > 34.4) across the sampling area in 2014 than in any other year. MLD was usually shallower than 20 m, and did not reach further than 30 m (Fig. 2d). Fig. 2. View largeDownload slide Horizontal and yearly variations in environmental parameters in the Sea of Japan: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a concentration and (f) water-column Chl a. The number within each rectangle denotes the year of sampling. Low sea surface height areas indicating anticyclonic eddies are shown by blue lines with the letter L inside encircled areas (b). Fig. 2. View largeDownload slide Horizontal and yearly variations in environmental parameters in the Sea of Japan: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a concentration and (f) water-column Chl a. The number within each rectangle denotes the year of sampling. Low sea surface height areas indicating anticyclonic eddies are shown by blue lines with the letter L inside encircled areas (b). SSChl a concentration was <1 μg L−1, except at Stn. 49, in 2015 (Fig. 2e). In 2011 and 2014, it was <0.25 μg L−1 across a wide area (0.13 ± 0.05 and 0.22 ± 0.17 μg L−1, respectively). It was three times higher in 2013 (0.39 ± 0.09 μg L−1) and 2015 (0.42 ± 0.17 μg L−1) than in 2011. Mean water-column chlorophyll a concentration at a depth of 10–100 m (water-column Chl a) concentration was spatially mismatched with SSChl a concentration, but they had a similar yearly variation (Fig. 2f). Similar to SSChl a concentration, the yearly mean values for water-column Chl a concentration were high in 2013 and 2015 (0.43 ± 0.09 and 0.46 ± 0.14 μg L−1, respectively). Zooplankton composition The sum of abundances of all appendicularian species ranged from 0 to 5403 inds m−3 (467 ± 632 inds m−3). They were the second most abundant zooplankton group after copepods. During the 5 years of our study, we observed six Oikopleura species, O. longicauda, O. fusiformis, O. dioica, O. rufescens, O. intermedia and O. labradoriensis (Fig. 3), and four Fritillaria species, F. borealis, F. formica, F. pellucida and F. tenella (Fig. 4). We observed two subspecies of F. borealis, F. borealis typica and F. borealis sargassi, with the latter making up on average 97% of the observations for the species. Some recorded Oikopleura and Fritillaria could not be identified to species level because key body parts were broken. At three stations (Stns 13 and 14 in 2011 and Stn. 14 in 2012), appendicularians were not observed. Fig. 3. View largeDownload slide Horizontal and yearly variations in the genus Oikopleura in the Sea of Japan: (a) O. longicauda; (b) O. fusiformis; (c) O. dioica; (d) O. rufescens (open circle), O. intermedia (grey circle) and O. labradoriensis (closed circle); and (e) unidentified Oikopleura. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Fig. 3. View largeDownload slide Horizontal and yearly variations in the genus Oikopleura in the Sea of Japan: (a) O. longicauda; (b) O. fusiformis; (c) O. dioica; (d) O. rufescens (open circle), O. intermedia (grey circle) and O. labradoriensis (closed circle); and (e) unidentified Oikopleura. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Fig. 4. View largeDownload slide Horizontal and yearly variations in the genus Fritillaria in the Sea of Japan: (a) F. borealis, (b) F. formica, (c) F. pellucida, (d) F. tenella and (e) unidentified Fritillaria. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Fig. 4. View largeDownload slide Horizontal and yearly variations in the genus Fritillaria in the Sea of Japan: (a) F. borealis, (b) F. formica, (c) F. pellucida, (d) F. tenella and (e) unidentified Fritillaria. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Among appendicularians, O. longicauda was the most abundant (271 ± 298 inds m−3; Fig. 3). It was the most abundant in 220 of 232 samples (excluding samples from the three stations where appendicularians were absent). The log-transformed abundance of O. longicauda had a normal distribution (Shapiro–Wilk test, P = 0.4). In the remaining 12 samples, F. borealis or F. formica was the most abundant species (7 and 5 samples, respectively; Fig. 4). Other species whose mean densities were over 10 inds m−3 were F. formica (30 ± 136 inds m−3), F. borealis (30 ± 224 inds m−3) and O. fusiformis (12 ± 76 inds m−3). Unidentified Fritillaria and Oikopleura also had relatively large abundances (56 ± 154 and 54 ± 114 inds m−3, respectively). The copepod Oithona (mainly O. similis and O. nana) was the most abundant zooplankton genus (1770 ± 917 inds m−3, including their copepodite stages) in our observation area (Fig. 5). The second to fifth most abundant zooplankton genera were the copepods Clausocalanus (887 ± 885 inds m−3, mostly C. pergens and its copepodite stages), Paracalanus (702 ± 604 inds m−3, mostly P. parvus s.l. and its copepodite stages), Oncaea (489 ± 382 inds m−3, mostly O. media and O. venusta, and their copepodite stages) and Microsetella (318 ± 221 inds m−3, M. norvegica and M. rosea and their copepodite stages). The numbers of Oncaea and Microsetella adults were 202 ± 192 and 253 ± 200 inds m−3, respectively: the proportions of adults to all were 40 ± 24% and 75 ± 24%, respectively. The cladocerans Penilia avirostris and Evadne and the carnivore zooplankton Sagitta were also present in relatively high numbers (181 ± 441, 68 ± 120 and 44 ± 52 inds m−3, respectively). Fig. 5. View largeDownload slide Horizontal and yearly variations in major zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Penilia avirostris, (g) Evadne and (h) Sagitta. The area of each circle denotes abundance and a reference scale for abundance is shown for each genus in the panels for 2015. A cross indicates that abundance was 0. Fig. 5. View largeDownload slide Horizontal and yearly variations in major zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Penilia avirostris, (g) Evadne and (h) Sagitta. The area of each circle denotes abundance and a reference scale for abundance is shown for each genus in the panels for 2015. A cross indicates that abundance was 0. We compared the abundances of the eight most common zooplankton genera (Oithona, Clausocalanus, Paracalanus, Oncaea, Microsetella, Evadne, Penilia and Sagitta) with that of O. longicauda. We found significant positive relationships (t-test P < 0.05, n = 232) between the abundance of O. longicauda and the abundances of Paracalanus, Oncaea, Microsetella, Penilia and Sagitta (Fig. 6). The positive relationship between Oncaea and Microsetella abundances was particularly strong (Fig. 6). Fig. 6. View largeDownload slide Relationships between the abundance of Oikopleura longicauda and the abundances of the eight most common zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Evadne, (g) Penilia and (h) Sagitta over 5 years. The three stations where O. longicauda was absent were removed from these plots. The line in panels (c), (d), (e), (g) and (h) indicates a statistically significant linear relationship between abundances of the two species (not log-transformed ones). Fig. 6. View largeDownload slide Relationships between the abundance of Oikopleura longicauda and the abundances of the eight most common zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Evadne, (g) Penilia and (h) Sagitta over 5 years. The three stations where O. longicauda was absent were removed from these plots. The line in panels (c), (d), (e), (g) and (h) indicates a statistically significant linear relationship between abundances of the two species (not log-transformed ones). Relationships between environmental variables and the abundance of Oikopleura longicauda Horizontal distribution of appendicularians was patchy with relatively high abundance at stations near the coast (Figs 3 and 4). There was also significant annual variation in abundance; yearly mean abundance was the highest in 2013 for all species [analysis of variance (ANOVA) test, P < 0.05], with the exception of O. dioica, O. intermedia, O. labradoriensis and F. borealis. In particular, the mean abundance of O. longicauda was the highest in 2013 (472 ± 487 inds m−3; ANOVA with post hoc Tukey HSD test, P < 0.05); it was approximately one-third of this value in both 2011 (182 ± 150 inds m−3) and 2014 (165 ± 95 inds m−3). Based on model selection using BIC for relationships between appendicularian abundance and hydrographic and other variables (SST, water-column T, SSS, water-column S, MLD, SSChl a, water-column Chl a, depth, year and time), water-column T and year were the best predictors of O. longicauda abundance. The r2 value for the best-fit model was 0.233. Coefficients for standardized water-column T were positive (mean ± SE: 0.114 ± 0.023): when using water-column T before standardization, the coefficient was 0.0616 ± 0.0126. These relationships were confirmed by simple linear relationships (Fig. 7); common logarithm-transformed abundance of O. longicauda was positively related to water-column T. Fig. 7. View largeDownload slide Relationships between common log-transformed Oikopleura longicauda abundance and environmental parameters: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a and (f) water-column Chl a. The grey line in panels (b) and (c) indicates a statistically significant relationship. Fig. 7. View largeDownload slide Relationships between common log-transformed Oikopleura longicauda abundance and environmental parameters: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a and (f) water-column Chl a. The grey line in panels (b) and (c) indicates a statistically significant relationship. DISCUSSION Summer abundance of zooplankton in the Sea of Japan Appendicularians, in particular O. longicauda, are one of the most important zooplankton groups in the southern Sea of Japan during the summer. In our study, they were the second most abundant group after copepods, and the appendicularian genus Oikopleura was the sixth most abundant genus after the copepod genera Oithona, Clausocalanus, Paracalanus, Oncaea and Microsetella (Figs 3 and 5). The dominance of O. longicauda is consistent to Tomita et al. (2003), who investigated in the Toyama Bay. We found that F. formica and F. borealis were the second most abundant appendicularian species, with their mean abundances ~30 inds m−3 (Fig. 4). However, F. formica remained at <10 inds m−3 throughout the year in Toyama Bay (Tomita et al., 2003). In our study, Oikopleura dioica was observed infrequently, and its maximum abundance was 200 inds m−3 (Fig. 3c), although it was the dominant species in the Seto Inland Sea, which adjoins the Sea of Japan (Uye and Ichino, 1995; Nakamura et al., 1997; Nakamura, 1998), and the East China Sea (Xu and Zhang, 2010). Conditions of the pelagic zone in the southern part of the Sea of Japan, where the Tsushima Warm Current flows, are affected largely by the water conditions in the East China Sea (which itself is affected by Changjiang Diluted Water), the Taiwan Warm Current and the Kuroshio, especially during the summer (Kodama et al., 2015; Kodama et al., 2016). In the western part of the East China Sea, whose water flows into the Sea of Japan, the abundance of O. dioica (with a summer mean of 1.4 × 103 inds m−3 (Xu and Zhang, 2010) was similar to that of O. longicauda. On the other hand, in the Kuroshio, which is one of the origins of the Tsushima Warm Current, O. longicauda was found to be the most dominant species, in a study conducted in winter and early spring (Hidaka, 2008). The results of our study show that the appendicularian component of the Sea of Japan was similar to that of the Kuroshio. Our results are also match up with Lombard et al. (2010): they estimate the O. longicauda dominance in the summer Sea of Japan using satellite Chl a concentration and temperature. Environmental factors influencing Oikopleura longicauda abundance The results of GLM indicate that water-column T was the best predictor of O. longicauda abundance. In O. dioica, generation time decreases with increasing temperature to an upper limit of between 26°C (Sato et al., 2003) and 29°C (Hopcroft and Roff, 1995). Estimated optimum temperature and salinity are similar for O. dioica (23.9 and 33.8 °C) and O. longicauda (25.2 and 33.6 °C) in the East China Sea (Xu and Zhang, 2010). López-Urrutia et al. (2005) recorded abundance for O. longicauda peaking at 24.5°C, the maximum temperature in European coastal waters. This suggests that O. longicauda grows rapidly in warm water, and may do so faster than O. dioica, whose abundance peaked at 9.5°C in European seas (López-Urrutia et al., 2005). In the East China Sea, O. longicauda abundance peaked at 24–26°C (Xu and Zhang, 2010), values were well within the summer SST range (22–28°C; Fig. 2a) that we observed in the Sea of Japan. Therefore, it is highly likely that the warm water conditions in our study site enhanced the growth of O. longicauda resulting in high abundance. In contrast, there was no positive relationship between Chl a concentration (the index of food concentration) and O. longicauda abundance. Studies on food concentration and appendicularian physiology are limited to O. dioica, and they show an increase of growth rate and body size saturated under the eutrophic conditions (Troedsson et al., 2002; Touratier et al., 2003; Lombard et al., 2009a), which also causes increased egg production (Troedsson et al., 2002; Nishida, 2008). Oikopleura longicauda is more abundant in oligotrophic conditions than O. dioica (Lombard et al., 2010), suggesting that the Chl a at our study site (0.4 μg L−1) may have been sufficient for O. longicauda. Abundance of predators also did not have large effects on the abundance of O. longicauda. Sagitta is a major predator of appendicularians (Alldredge, 1976b). However, in our study, the abundance of Sagitta, and that of other zooplankton, was positively correlated with that of O. longicauda (Fig. 6): the abundance of prey may determine the abundance of Sagitta, with the lower trophic level structuring the food chain. Thermohaline conditions were the most important factor determining the abundance of O. longicauda in the Sea of Japan. The factors influencing yearly variation in appendicularian abundance are not clear, but it is possible that the yearly variations in appendicularian abundances are related to these variations in water characteristics. Annual variations in chemical and physical characteristics of water have been observed in the Tsushima Strait where the Tsushima Warm Current originates, and the less saline water originating in Changjiang was widely distributed at the Tsushima Strait in the summer of 2013 (Kodama et al., 2017b). The negative relationship between water-column S and abundance of O. longicauda (Fig. 7) could support this, while water column S was not picked up as the explanatory factor in GLM. The role of Oikopleura longicauda in the ecosystem The abundance of O. longicauda is considered to peak in midsummer when temperature is more elevated based on the relationship to the temperature. This is consistent with the findings of Chiba and Saino (2003) who reported that appendicularian abundance increased during the summer in the Sea of Japan. Appendicularians are eaten by fish larvae in our study area (Kodama et al., 2017a). Given that the abundance of copepods is low in the summer due to low Chl a concentrations (Chiba and Saino, 2003; Iguchi, 2004), O. longicauda may have a relatively more important role in the diets of zooplanktivorous fish during the summer than during other seasons. Microsetella and Oncaea are well known as grazers of discarded appendicularian houses (Ohtsuka and Kubo, 1991; Ohtsuka et al., 1993; Koski et al., 2007; Nishibe et al., 2015). Therefore, the increase in abundance of O. longicauda may have improved the feeding environment for Oncaea and Microsetella, resulting in increases in abundances of the two copepod taxa (Fig. 6). We can estimate the carbon flux represented by house production by O. longicauda and house ingestion by Oncaea and Microsetella. The carbon content of the discarded house (CDH) is positively correlated with size (trunk length, LT) and body carbon content (CB) of the appendicularian (Sato et al., 2003). We estimated CB of O. longicauda by the following equation in Sato et al. (2003): CB[μgind−1]=3.29×10−8LT2.85 (1) Size was not measured in our study. Therefore, for the above calculation, we assume that LT of O. longicauda was 175 μm, based on the modal values for the species (150–200 μm) obtained by Tomita et al. (1999) in the Sea of Japan during the summer. We then calculate CDH as follows (Sato et al., 2003): CDH[μ ghouse-1]=0.179×CB (2) We ignore the effects of Chl a concentration in our calculation of CDH because the Chl a concentration of Sato et al. (2003) was within the range of concentrations in our study (Fig. 2f). The product of CDH and house renewal rate (RHR) gives an estimate of the total carbon content of houses discarded on an hourly basis by an O. longicauda individual. RHR does not depend on CB, but depends on temperature and salinity in the case of O. dioica (Sato et al., 2001), and the carbon content of new houses in the case of other Oikopleura species (Sato et al., 2003). For estimating RHR, we can use the simple linear regression for the relationship between daily house renewal rate and temperature given for O. dioica in Sato et al. (2001): RHR[houses h-1]=0.9739×T-2.8361 (3) Here, we use mean water-column T as T, since the abundance of O. longicauda had a significant positive relationship with water-column T, but no relationship with SST. Although temperature varied widely in our study, salinity did not (Fig. 2); we, therefore, ignore the effect of the latter. Since the unidentified Oikopleura were significantly observed in our study, we regarded their abundances as O. longicuda in the estimation. Feeding rates of Oncaea and Microsetella can be estimated based on the literature values (Koski et al., 2007; Nishibe et al., 2015). The ingestion rate for Oncaea was calculated only for adults (after removing copepodite numbers from abundance values) as 0.3 μg C ind−1 d−1 based on Nishibe et al. (2015) results for the Kuroshio region; a rate intermediate between those in Koski et al. (2007), 0.2 μg C ind−1 d−1 and Alldredge (1972), 2.8 μg C ind−1 d−1, and the water temperature is the same level with our study. The ingestion rate for Microsetella was set as 0.02 μg C ind−1 d−1 for adults based on Koski et al. (2007) for M. norvegica. In our area, both M. norvegica and M. rosea, which is bigger than M. norvegica and attaches to discarded appendicularian houses (Steinberg et al., 1994), were present. On the basis of the assumptions and calculations above, the daily carbon content of discarded houses ranged 0–60.9 mg C m−2 d−1 (mean ± SD: 7.7 ± 7.8 mg C m−2 d−1) for O. longicauda in our study. This was within the ranges for Toyama Bay (0.11–266 mg C m−2 d−1 (Tomita et al., 1999), the Kuroshio off Honshu in early spring (7.4–8.1 mg C m−2 d−1 in the 0–150 m layer (Hidaka, 2008) and Tokyo Bay (3.6–508 mg C m−2 d−1 in the 0–25 m layer (Sato et al., 2008). The potential carbon ingestion rates for Oncaea and Microsetella were 10.6 ± 9.3 and 0.70 ± 0.55 mg C m−2 d−1, respectively. Our estimation is similar to oncaeid ingestion rates in an earlier study of the Kuroshio, 12.3–31.3 mg C m−2 d−1 (Nishibe et al., 2015). Summed carbon ingestion rates for Oncaea and Microsettela (community ingestion rate) were higher than the amount of carbon available in houses discarded daily by O. longicauda, assuming Oncaea and Microsettela feed only on discarded houses. However, this simple community ingestion rate is probably an overestimate, as Nishibe et al. (2015) reported a maximum of only 34% of Oncaea attaching to discarded houses. When factored into the community ingestion rate, this maximum percentage attachment gives a re-calculated community ingestion rate of 3.9 ± 3.3 mg C m−2 d−1, which is half of the daily amount available in house discards. At 59 of 235 stations, the community ingestion rate was estimated to be in excess of the C available through house discards. In particular, it was higher at 26 of 49 stations in 2012, and only at four stations in 2013 when the abundances of O. longicauda were significantly high. In addition, the discarded houses of O. longicauda sink 190 m d−1 (Taguchi, 1982), and Oncaea is distributed mainly at 25 m depth, and observed from 0 to 50 m depth in Toyama Bay in the Sea of Japan (Takahashi and Uchiyama, 2008). If the vertical distribution of Oncaea is assumed to be limited to a depth of <50 m, the period during which discarded houses are potentially available for ingestion is <6 h; therefore, the daily ingestion rate may remain 0.97 ± 0.82 mg C m−2 d−1, corresponding to one-eighth of the amount of C available through daily house discards. The presence of copepodites and nauplii of Oncaea provides a possible explanation of the underestimation of the community ingestion rate: the number of copepodites was higher than adults on average, and the feeding habitats of these larvae are not clear. These results suggest that zooplankton consume 12.5–100% of houses discarded daily by O. longicauda during summer in the Sea of Japan. Compared to ingestion rates for oncaeids (~10% d−1 of discarded house biomass) in other marine environments (Steinberg et al., 1997; Koski et al., 2007; Nishibe et al., 2015), our estimations are considered high, while yearly variation of our study area was observed. The strong correlations between abundances of Microsettela or Oncaea and O. longicauda may be explained by the high ingestion rates; the abundances of these two copepod species are considered to be controlled by their food supply. Interestingly, Oncaea venusta reproduce actively in warm conditions in the Sea of Japan (Hirakawa, 1995), while phytoplankton abundance is low in such waters; this may be related to the abundance of O. longicauda, which also increases in warm waters, as shown in this study. Discarded appendicularian houses are not only consumed by Oncaea and Microsettela but also by heterotrophs such as bacteria, ciliates, crustacean nauplii and polychaetes (Kiørboe, 2001). Further studies are necessary to evaluate the abundance of discarded appendicularian houses and their importance for carbon cycling in marine ecosystems, particularly in the deeper zones of the ocean, because rapid lowering of pH with increasing CO2 concentrations occurs in the deeper layers of the Sea of Japan (Chen et al., 2017). CONCLUSIONS A 5-year survey was conducted to assess the abundances of appendicularians and other zooplankton in the Sea of Japan. Ten appendicularian species were recorded. Of those, Oikopleura longicauda was the most dominant throughout the area studied. Its abundance was positively related to habitat temperature and was three times higher in 2013 than in 2014. Abundances of other appendicularians were also high in 2013. However, the reason for yearly variation is not clear in the present study. There was a positive relationship between the abundance of O. longicauda and the abundances of Microsetella and Oncaea, which feed on discarded appendicularian houses: the high abundance of O. longicauda may have positively affected these two copepod taxa. In addition, abundance of the carnivorous Sagitta was also strongly correlated with that of O. longicauda. Therefore, not only O. longicauda bodies but also their discarded houses are an important link in the transfer of energy from primary to higher trophic levels in the epipelagic ecosystem in the Sea of Japan during summer, and contribution to carbon sinking will be further studied. SUPPLEMENTARY DATA Supplementary data can be found online at Journal of Plankton Research online. ACKNOWLEDGEMENTS Samples were collected during cruises of RV Shunyo-Maru and Shoyo-Maru of the Japan Fisheries Research and Education Agency and Fisheries Agency, respectively, and we thank the captains, crews, and many researchers during the cruises. We deeply appreciate Dr K. Hidaka for providing valuable advice, Mr T. Takahashi for copepods identification and Dr S. Furukawa for advising statistics. We also acknowledge an anonymous reviewer and Dr F. Lombard for their insightful comments. FUNDING This work was financially supported by Fisheries Agency of Japan, and Japan Fisheries Research and Education Agency, and JSPS (Japan Society for the Promotion of Science) KAKENHI Grant-in-Aid for Scientific Research grant (16K07831) for T.K. REFERENCES Alldredge , A. L. ( 1972 ) Abandoned larvacean houses: a unique food source in the pelagic environment . Science , 177 , 885 – 887 . Google Scholar CrossRef Search ADS PubMed Alldredge , A. L. 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Appendicularians in the southwestern Sea of Japan during the summer: abundance and role as secondary producers

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Abstract

Abstract Appendicularian abundance was investigated at a total of 235 stations over 5 years, from 2011 to 2015, in southwestern Sea of Japan to evaluate potential factors influencing abundance and to understand their effects on the marine ecosystem. Oikopleura longicauda was the dominant appendicularian species, present in 232 samples, and with the highest abundance (mean ± SD: 463 ± 694 individuals m−3) among the appendicularians. Warm conditions appear to favour O. longicauda based on a generalized linear model, and salinity and chlorophyll a concentration were not significantly related to abundance. The abundance of O. longicauda was correlated significantly with those of Microsetella and Oncaea, which are the grazers of discarded appendicularian houses, as well as that of carnivorous Sagitta. Oikopleura longicauda houses, discarded daily to the water column, were estimated to represent a carbon flux of 7.7 ± 7.8 mg C m−2 d−1 (mean ± SD), depending on their density and water temperature. We estimate that a minimum of approximately 13% of houses were consumed by Oncaea and Microsettela. Therefore, we suggest that secondary production by O. longicauda in the southwestern Sea of Japan increased during summer and leads to enriched production at higher trophic levels in the epipelagic ecosystem during this season. INTRODUCTION Appendicularians, or larvaceans (Tunicata: Appendicularia), are cosmopolitan secondary producers and are the second most dominant zooplankton group in the world’s oceans. They are found, irrespective of warm or cold temperatures, in coastal zones and the open ocean, in eutrophic or oligotrophic waters (López-Urrutia et al., 2003; Steinberg et al., 2008; Jaspers et al., 2009). They are filter feeders and use a specialized outer casing or “house”, made by secreting mucus and cellulose, to filter and concentrate small food particles (Alldredge, 1976b). Once it becomes clogged with uneaten food particles and waste, the house is shed and a new house is secreted (Alldredge, 1976b). This feeding strategy is generally considered advantageous in oligotrophic oceans (López-Urrutia et al., 2003). Appendicularians discard 2–40 houses day−1, taking <5 min to rebuild a new house (Sato et al., 2001, 2003). Both appendicularians and their discarded houses play important roles in biological production and carbon cycling in oceans (Alldredge, 1972, 1976a; Robison et al., 2005). Appendicularian contribution to mesozooplankton secondary production increases with increasing productivity of the environment, and they are estimated to consume 8% of annual primary production in European coastal waters (López-Urrutia et al., 2003). Appendicularians are an important source of food for many fish species and zooplankton, such as the sergeant major, medusae, chaetognaths and ctenophores (Alldredge, 1976b). A large number of studies report that appendicularins are important food for carnivore medusae and various life stages of fish (Purcell et al., 2005). In Japanese coastal waters, larvae of flounders, Pleuronichthys cornutus, Pseudorhombus pentophthalmus and Paralichthys olivaceus, feed on appendicularians (Kuwahara and Suzuki, 1983; Ikewaki and Tanaka, 1993; Hasegawa et al., 2003). Larvae and juveniles of the Japanese sardine, Sardinops melanostictus, are also reported to be grazers of appendicularians (Watanabe and Saito, 1998), as are those of the red sea beam, Pagrus major (Shimamoto and Watanabe, 1994). A metagenetic study found that the larvae of the Pacific bluefin tuna, Thunnus orientalis, which spawns during the summer in southwestern Sea of Japan (Ohshimo et al., 2017), feed selectively on appendicularians (Kodama et al., 2017a). The discarded appendicularian houses, which sink rapidly through the water column, are an important component of marine snow (Hansen et al., 1996; Robison et al., 2005), and make a considerable input to carbon cycling in the oceans. Leptocephali of eight eel species feed selectively on appendicularian houses (Mochioka and Iwamizu, 1996). Both abandoned and occupied houses are an important source of food for pelagic copepods, such as Scolecithrix danae, Microsetella spp. and Oncaea spp., which are known to attach themselves to the houses prior to feeding on them (Ohtsuka and Kubo, 1991; Ohtsuka et al., 1993; Nishibe et al., 2015). The distribution and the abundance of appendicularians are usually related to temperature, salinity, food concentration and grazing pressure (Shiga, 1985; Taggart and Frank, 1987; Tomita et al., 2003; Shiganova, 2005; Hidaka, 2008; Lombard et al., 2010; Xu and Zhang, 2010). Regardless of species, increases in temperature in the optimal temperature range (~30°C) promote house renewal rates (Sato et al., 2001, 2003), enhance growth (López-Urrutia et al., 2003) and shorten appendicularian generation times (Sato et al., 2001; López-Urrutia et al., 2003; Lombard et al., 2009b; Deibel and Lowen, 2012). Increases in salinity decrease house renewal rates (Sato et al., 2001). Food concentration studies are limited to data on O. dioica and show that minimally constrained food concentrations (30 μg C L−1) restrict appendicularian body sizes (Touratier et al., 2003; Lombard et al., 2009a) and decrease growth rates (Troedsson et al., 2002). Growth rates adhere to a maximum upper limit under conditions of sufficient food (López-Urrutia et al., 2003; Lombard et al., 2009b; Deibel and Lowen, 2012). House renewal rates are also affected by food concentration (Fenaux, 1985; Selander and Tiselius, 2003; Tiselius et al., 2003); renewal rates only increase with concentration at low concentrations (Selander and Tiselius, 2003; Tiselius et al., 2003). Sato et al. (2001), however, showed that mean house renewal rates did not differ significantly under different food concentrations. Rather, food concentration significantly affected egg numbers (Troedsson et al., 2002; Nishida, 2008). Although temperature and availability of food may increase appendicularian abundance, these relationships are non-linear (Hidaka, 2008; Xu and Zhang, 2010). Moreover, Lombard et al. (2010) showed that appendicularian optimal food and temperature conditions are species-specific: O. longicauda is adapted to oligotrophic conditions; O. dioica prefers colder water than O. fusiformis and O. rufescens. In one of the few studies on predation pressure on appendicularians, Shiganova (2005) found that the abundance of Oikopleura dioica fell after invasion by a predator, the ctenophore Mnemiopsis leidyi, in the Black Sea. Appendicularians are one of the major zooplankton groups in the Sea of Japan, the semi-closed marginal sea in the western North Pacific (Tomita et al., 1999, 2003), and their abundance varies with the seasonal cycle of phytoplankton abundance in the Sea (Tomita et al., 2003). However, previous studies on appendicularians in the area were limited to Toyama Bay, where the summer phytoplankton bloom occurs due to river discharge (Terauchi et al., 2014). Additionally, the Changjiang discharged water, Kuroshio water and Taiwan Warm Current water are the sources of the Tsushima Warm Current, which flow in the southern part of the Sea of Japan (Senjyu et al., 2008). Therefore, the species composition and the abundance of appendicularians may be different horizontally with hydrographic and other environmental variables. Given that appendicularians are important prey items for fish and other organisms, an assessment of their abundance during summer is essential for understanding trophic relationships in the Sea of Japan. Therefore, we conducted surveys for 5 years to examine appendicularian abundance and species composition in the southwestern part of the Sea. We used a generalized linear model to evaluate environmental factors with potential to cause fluctuations in the abundance of appendicularians. We also considered the role of appendicularians as secondary producers in the Sea of Japan. METHODS Observations Oceanic observations were conducted in July, from 2011 to 2015, on board R/V Shunyo-Maru, Japan Fisheries Research and Education Agency (2011, 2014 and 2015), and R/V Shoyo-Maru, Fisheries Agency (2012 and 2013), at 49 stations (Stns 1–49) set every 10 or 15 nautical miles along five line transects (named A–E) in the southwestern Sea of Japan (Fig. 1). During the 2011 cruise, Stns 41–49 were not observed because of a shortage in ship time. Fig. 1. View largeDownload slide Map of sampling stations in the Sea of Japan. Open circles and numbers within them denote station positions and station numbers, respectively. Letters A–E denote different line transects. The grey shadow along the coast indicates the continental shelf. Fig. 1. View largeDownload slide Map of sampling stations in the Sea of Japan. Open circles and numbers within them denote station positions and station numbers, respectively. Letters A–E denote different line transects. The grey shadow along the coast indicates the continental shelf. At every station, vertical profiles of temperature and salinity were recorded using a conductivity–temperature–depth (CTD) sensor (SBE 9plus, Sea-Bird Scientific) with an in vivo chlorophyll (Chl) fluorescence sensor (ECO-AFL/FL, WET Labs, during the Shunyo-Maru cruises, and Chlorophyll Fluorometer, Seapoint, during the Shoyo-Maru cruises) and a carousel water sampling system (SBE 32, Sea-Bird Scientific) from ~5 to 500 m depth or 10 m above the bottom. Hydrographic data used in our study were obtained from depths <100 m because most of the appendicularians are present in the Sea of Japan at these depths (Tomita et al., 2003). At Stns 1 and 44, the depth of the sea bottom was <100 m; therefore, hydrographic data were obtained from depths shallower than this. For sea surface temperature (SST), seawater was sampled with a bucket and temperature measured with a calibrated mercury thermometer. Mixed layer depth (MLD) was determined based on the potential density criterion 0.125 (Levitus, 1982). Weekly mean sea surface height was derived from Ssalto/Duacs gridded absolute dynamic topography (www.aviso.altimetry.fr) for confirmation of mesoscale eddies. Water was sampled from the surface with a bucket at every station. The carousel water sampling system was used for discrete vertical sampling at odd numbered stations (20 stations in 2011 and 25 stations after 2012). For evaluating the vertical profile of Chl a concentration, water was collected at 11 depths above 200 m, particles in 300 mL of seawater were collected on a glass fibre filter (GF/F, Whatman), and the concentration was measured with a fluorometer (TD-700, Turner Designs, during the 2011–2013 cruises, and 10 AU during the 2014 and 2015 cruises) after extraction (Welschmeyer, 1994). For these data, in vivo Chl fluorescence was calibrated at every cruise regardless of time of day (r2 > 0.86). In vivo Chl fluorescence has a diel rhythm (Holm-Hansen et al., 2000); however, we ignored this because significant differences in diel slopes were observed only during the 2014 cruise (t-test, P = 0.03). Zooplankton were collected with vertical hauls of a long North Pacific standard plankton (Norpac) net (Nytal 13XX, 100 μm mesh, 0.45 m mouth diameter, Rigo) up to the surface from a depth of 200 m or from 10 m above the bottom. A flow metre (Rigo), calibrated after every cruise, was installed at the mouth of the net in order to estimate the volume of filtered water. Zooplankton samples were fixed with neutral formalin soon after sampling, and stored at room temperature until morphological identification. Individuals were identified to the lowest taxonomic level, and the abundance of each zooplankton species was calculated using counts of each species and water volume in each station (individuals per cubic metre, inds m−3). Statistical analyses The environmental factors affecting appendicularian abundances were evaluated with a generalized linear model (GLM), using the package “MASS” (Venables and Ripley, 2013) in R version 3.4.0 (R Core Team, 2017). We selected the best model based on the Bayesian information criterion (BIC); ΔBIC was calculated as the difference between the full model containing all covariates and the null model (intercept only) using “dredge” function in the “MuMin” package of R. The response variable was the common log-transformed abundance of each appendicularian species. The explanatory variables were SST, mean temperature from a depth of 10 to 100 m (water-column T), sea surface salinity (SSS), mean salinity from a depth of 10 to 100 m (water-column S), sea surface Chl a (SSChl a), mean Chl a from a depth of 10 to 100 m (water-column Chl a), MLD, haul depth (depth), year and time. Depth (shallow: <100 m; middle: 100–200 m; and deep: ≥200 m), year and time (divided twice-hourly) were categorical variables, while the other parameters were continuous variables and linked with linear functions. The continuous variables were standardized to 0 mean and 1 variance using the “vegan” package in R. We applied these analyses to the species which was present in ≥50% of the stations and whose abundance was normally or log-normally distribution. Normality of abundance data was tested with the Shapiro–Wilk test. We evaluated the environmental factors affecting appendicularian abundances with a generalized additive model (GAM) using the “mgcv” package; however, the BIC in the GLM was smaller than those of GAM, and the GLM was selected as the best-suited model. RESULTS Hydrography SST ranged 22–28°C in all sampling years (Fig. 2a). High SST values were observed across a wide area in 2014 (mean ± SD: 25.1 ± 0.8°C), while they were lower in 2013 and 2015 (23.4 ± 0.8°C in both years, Fig. 2a) than in 2014. In 2011, SSTs were higher in line B (Fig. 2a) than in other lines. Variations in water-column T (between 10 and 100 m depth) were different from those in SST (Fig. 2b). Water-column T was high (~15°C) near the coast of Honshu, for example at Stns 22 and 23, and low in the cyclonic eddies identified as low sea surface height (Fig. 2b). The high water-column T at Stns 1 and 44 reflected the shallow bottom at these stations. Yearly mean water-column T in the area was the highest in 2013 (18.0 ± 1.9°C) and the second highest in 2014 (17.4 ± 1.8°C). Generally, variations in mean water-column salinity at a depth of 10–100 m (water-column S) corresponded to variations in water-column T (Fig. 2c); salinity was low at stations where water-column T was low except in the coastal areas. Water-column S was higher (by > 34.4) across the sampling area in 2014 than in any other year. MLD was usually shallower than 20 m, and did not reach further than 30 m (Fig. 2d). Fig. 2. View largeDownload slide Horizontal and yearly variations in environmental parameters in the Sea of Japan: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a concentration and (f) water-column Chl a. The number within each rectangle denotes the year of sampling. Low sea surface height areas indicating anticyclonic eddies are shown by blue lines with the letter L inside encircled areas (b). Fig. 2. View largeDownload slide Horizontal and yearly variations in environmental parameters in the Sea of Japan: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a concentration and (f) water-column Chl a. The number within each rectangle denotes the year of sampling. Low sea surface height areas indicating anticyclonic eddies are shown by blue lines with the letter L inside encircled areas (b). SSChl a concentration was <1 μg L−1, except at Stn. 49, in 2015 (Fig. 2e). In 2011 and 2014, it was <0.25 μg L−1 across a wide area (0.13 ± 0.05 and 0.22 ± 0.17 μg L−1, respectively). It was three times higher in 2013 (0.39 ± 0.09 μg L−1) and 2015 (0.42 ± 0.17 μg L−1) than in 2011. Mean water-column chlorophyll a concentration at a depth of 10–100 m (water-column Chl a) concentration was spatially mismatched with SSChl a concentration, but they had a similar yearly variation (Fig. 2f). Similar to SSChl a concentration, the yearly mean values for water-column Chl a concentration were high in 2013 and 2015 (0.43 ± 0.09 and 0.46 ± 0.14 μg L−1, respectively). Zooplankton composition The sum of abundances of all appendicularian species ranged from 0 to 5403 inds m−3 (467 ± 632 inds m−3). They were the second most abundant zooplankton group after copepods. During the 5 years of our study, we observed six Oikopleura species, O. longicauda, O. fusiformis, O. dioica, O. rufescens, O. intermedia and O. labradoriensis (Fig. 3), and four Fritillaria species, F. borealis, F. formica, F. pellucida and F. tenella (Fig. 4). We observed two subspecies of F. borealis, F. borealis typica and F. borealis sargassi, with the latter making up on average 97% of the observations for the species. Some recorded Oikopleura and Fritillaria could not be identified to species level because key body parts were broken. At three stations (Stns 13 and 14 in 2011 and Stn. 14 in 2012), appendicularians were not observed. Fig. 3. View largeDownload slide Horizontal and yearly variations in the genus Oikopleura in the Sea of Japan: (a) O. longicauda; (b) O. fusiformis; (c) O. dioica; (d) O. rufescens (open circle), O. intermedia (grey circle) and O. labradoriensis (closed circle); and (e) unidentified Oikopleura. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Fig. 3. View largeDownload slide Horizontal and yearly variations in the genus Oikopleura in the Sea of Japan: (a) O. longicauda; (b) O. fusiformis; (c) O. dioica; (d) O. rufescens (open circle), O. intermedia (grey circle) and O. labradoriensis (closed circle); and (e) unidentified Oikopleura. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Fig. 4. View largeDownload slide Horizontal and yearly variations in the genus Fritillaria in the Sea of Japan: (a) F. borealis, (b) F. formica, (c) F. pellucida, (d) F. tenella and (e) unidentified Fritillaria. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Fig. 4. View largeDownload slide Horizontal and yearly variations in the genus Fritillaria in the Sea of Japan: (a) F. borealis, (b) F. formica, (c) F. pellucida, (d) F. tenella and (e) unidentified Fritillaria. The area of each circle denotes abundance and a reference scale for abundance is shown for each species in the panels for 2015. A cross indicates that abundance was 0. Among appendicularians, O. longicauda was the most abundant (271 ± 298 inds m−3; Fig. 3). It was the most abundant in 220 of 232 samples (excluding samples from the three stations where appendicularians were absent). The log-transformed abundance of O. longicauda had a normal distribution (Shapiro–Wilk test, P = 0.4). In the remaining 12 samples, F. borealis or F. formica was the most abundant species (7 and 5 samples, respectively; Fig. 4). Other species whose mean densities were over 10 inds m−3 were F. formica (30 ± 136 inds m−3), F. borealis (30 ± 224 inds m−3) and O. fusiformis (12 ± 76 inds m−3). Unidentified Fritillaria and Oikopleura also had relatively large abundances (56 ± 154 and 54 ± 114 inds m−3, respectively). The copepod Oithona (mainly O. similis and O. nana) was the most abundant zooplankton genus (1770 ± 917 inds m−3, including their copepodite stages) in our observation area (Fig. 5). The second to fifth most abundant zooplankton genera were the copepods Clausocalanus (887 ± 885 inds m−3, mostly C. pergens and its copepodite stages), Paracalanus (702 ± 604 inds m−3, mostly P. parvus s.l. and its copepodite stages), Oncaea (489 ± 382 inds m−3, mostly O. media and O. venusta, and their copepodite stages) and Microsetella (318 ± 221 inds m−3, M. norvegica and M. rosea and their copepodite stages). The numbers of Oncaea and Microsetella adults were 202 ± 192 and 253 ± 200 inds m−3, respectively: the proportions of adults to all were 40 ± 24% and 75 ± 24%, respectively. The cladocerans Penilia avirostris and Evadne and the carnivore zooplankton Sagitta were also present in relatively high numbers (181 ± 441, 68 ± 120 and 44 ± 52 inds m−3, respectively). Fig. 5. View largeDownload slide Horizontal and yearly variations in major zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Penilia avirostris, (g) Evadne and (h) Sagitta. The area of each circle denotes abundance and a reference scale for abundance is shown for each genus in the panels for 2015. A cross indicates that abundance was 0. Fig. 5. View largeDownload slide Horizontal and yearly variations in major zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Penilia avirostris, (g) Evadne and (h) Sagitta. The area of each circle denotes abundance and a reference scale for abundance is shown for each genus in the panels for 2015. A cross indicates that abundance was 0. We compared the abundances of the eight most common zooplankton genera (Oithona, Clausocalanus, Paracalanus, Oncaea, Microsetella, Evadne, Penilia and Sagitta) with that of O. longicauda. We found significant positive relationships (t-test P < 0.05, n = 232) between the abundance of O. longicauda and the abundances of Paracalanus, Oncaea, Microsetella, Penilia and Sagitta (Fig. 6). The positive relationship between Oncaea and Microsetella abundances was particularly strong (Fig. 6). Fig. 6. View largeDownload slide Relationships between the abundance of Oikopleura longicauda and the abundances of the eight most common zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Evadne, (g) Penilia and (h) Sagitta over 5 years. The three stations where O. longicauda was absent were removed from these plots. The line in panels (c), (d), (e), (g) and (h) indicates a statistically significant linear relationship between abundances of the two species (not log-transformed ones). Fig. 6. View largeDownload slide Relationships between the abundance of Oikopleura longicauda and the abundances of the eight most common zooplankton taxa in the Sea of Japan: (a) Oithona, (b) Clausocalanus, (c) Paracalanus, (d) Oncaea, (e) Microsetella, (f) Evadne, (g) Penilia and (h) Sagitta over 5 years. The three stations where O. longicauda was absent were removed from these plots. The line in panels (c), (d), (e), (g) and (h) indicates a statistically significant linear relationship between abundances of the two species (not log-transformed ones). Relationships between environmental variables and the abundance of Oikopleura longicauda Horizontal distribution of appendicularians was patchy with relatively high abundance at stations near the coast (Figs 3 and 4). There was also significant annual variation in abundance; yearly mean abundance was the highest in 2013 for all species [analysis of variance (ANOVA) test, P < 0.05], with the exception of O. dioica, O. intermedia, O. labradoriensis and F. borealis. In particular, the mean abundance of O. longicauda was the highest in 2013 (472 ± 487 inds m−3; ANOVA with post hoc Tukey HSD test, P < 0.05); it was approximately one-third of this value in both 2011 (182 ± 150 inds m−3) and 2014 (165 ± 95 inds m−3). Based on model selection using BIC for relationships between appendicularian abundance and hydrographic and other variables (SST, water-column T, SSS, water-column S, MLD, SSChl a, water-column Chl a, depth, year and time), water-column T and year were the best predictors of O. longicauda abundance. The r2 value for the best-fit model was 0.233. Coefficients for standardized water-column T were positive (mean ± SE: 0.114 ± 0.023): when using water-column T before standardization, the coefficient was 0.0616 ± 0.0126. These relationships were confirmed by simple linear relationships (Fig. 7); common logarithm-transformed abundance of O. longicauda was positively related to water-column T. Fig. 7. View largeDownload slide Relationships between common log-transformed Oikopleura longicauda abundance and environmental parameters: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a and (f) water-column Chl a. The grey line in panels (b) and (c) indicates a statistically significant relationship. Fig. 7. View largeDownload slide Relationships between common log-transformed Oikopleura longicauda abundance and environmental parameters: (a) SST, (b) water-column T, (c) water-column S, (d) MLD, (e) SSChl a and (f) water-column Chl a. The grey line in panels (b) and (c) indicates a statistically significant relationship. DISCUSSION Summer abundance of zooplankton in the Sea of Japan Appendicularians, in particular O. longicauda, are one of the most important zooplankton groups in the southern Sea of Japan during the summer. In our study, they were the second most abundant group after copepods, and the appendicularian genus Oikopleura was the sixth most abundant genus after the copepod genera Oithona, Clausocalanus, Paracalanus, Oncaea and Microsetella (Figs 3 and 5). The dominance of O. longicauda is consistent to Tomita et al. (2003), who investigated in the Toyama Bay. We found that F. formica and F. borealis were the second most abundant appendicularian species, with their mean abundances ~30 inds m−3 (Fig. 4). However, F. formica remained at <10 inds m−3 throughout the year in Toyama Bay (Tomita et al., 2003). In our study, Oikopleura dioica was observed infrequently, and its maximum abundance was 200 inds m−3 (Fig. 3c), although it was the dominant species in the Seto Inland Sea, which adjoins the Sea of Japan (Uye and Ichino, 1995; Nakamura et al., 1997; Nakamura, 1998), and the East China Sea (Xu and Zhang, 2010). Conditions of the pelagic zone in the southern part of the Sea of Japan, where the Tsushima Warm Current flows, are affected largely by the water conditions in the East China Sea (which itself is affected by Changjiang Diluted Water), the Taiwan Warm Current and the Kuroshio, especially during the summer (Kodama et al., 2015; Kodama et al., 2016). In the western part of the East China Sea, whose water flows into the Sea of Japan, the abundance of O. dioica (with a summer mean of 1.4 × 103 inds m−3 (Xu and Zhang, 2010) was similar to that of O. longicauda. On the other hand, in the Kuroshio, which is one of the origins of the Tsushima Warm Current, O. longicauda was found to be the most dominant species, in a study conducted in winter and early spring (Hidaka, 2008). The results of our study show that the appendicularian component of the Sea of Japan was similar to that of the Kuroshio. Our results are also match up with Lombard et al. (2010): they estimate the O. longicauda dominance in the summer Sea of Japan using satellite Chl a concentration and temperature. Environmental factors influencing Oikopleura longicauda abundance The results of GLM indicate that water-column T was the best predictor of O. longicauda abundance. In O. dioica, generation time decreases with increasing temperature to an upper limit of between 26°C (Sato et al., 2003) and 29°C (Hopcroft and Roff, 1995). Estimated optimum temperature and salinity are similar for O. dioica (23.9 and 33.8 °C) and O. longicauda (25.2 and 33.6 °C) in the East China Sea (Xu and Zhang, 2010). López-Urrutia et al. (2005) recorded abundance for O. longicauda peaking at 24.5°C, the maximum temperature in European coastal waters. This suggests that O. longicauda grows rapidly in warm water, and may do so faster than O. dioica, whose abundance peaked at 9.5°C in European seas (López-Urrutia et al., 2005). In the East China Sea, O. longicauda abundance peaked at 24–26°C (Xu and Zhang, 2010), values were well within the summer SST range (22–28°C; Fig. 2a) that we observed in the Sea of Japan. Therefore, it is highly likely that the warm water conditions in our study site enhanced the growth of O. longicauda resulting in high abundance. In contrast, there was no positive relationship between Chl a concentration (the index of food concentration) and O. longicauda abundance. Studies on food concentration and appendicularian physiology are limited to O. dioica, and they show an increase of growth rate and body size saturated under the eutrophic conditions (Troedsson et al., 2002; Touratier et al., 2003; Lombard et al., 2009a), which also causes increased egg production (Troedsson et al., 2002; Nishida, 2008). Oikopleura longicauda is more abundant in oligotrophic conditions than O. dioica (Lombard et al., 2010), suggesting that the Chl a at our study site (0.4 μg L−1) may have been sufficient for O. longicauda. Abundance of predators also did not have large effects on the abundance of O. longicauda. Sagitta is a major predator of appendicularians (Alldredge, 1976b). However, in our study, the abundance of Sagitta, and that of other zooplankton, was positively correlated with that of O. longicauda (Fig. 6): the abundance of prey may determine the abundance of Sagitta, with the lower trophic level structuring the food chain. Thermohaline conditions were the most important factor determining the abundance of O. longicauda in the Sea of Japan. The factors influencing yearly variation in appendicularian abundance are not clear, but it is possible that the yearly variations in appendicularian abundances are related to these variations in water characteristics. Annual variations in chemical and physical characteristics of water have been observed in the Tsushima Strait where the Tsushima Warm Current originates, and the less saline water originating in Changjiang was widely distributed at the Tsushima Strait in the summer of 2013 (Kodama et al., 2017b). The negative relationship between water-column S and abundance of O. longicauda (Fig. 7) could support this, while water column S was not picked up as the explanatory factor in GLM. The role of Oikopleura longicauda in the ecosystem The abundance of O. longicauda is considered to peak in midsummer when temperature is more elevated based on the relationship to the temperature. This is consistent with the findings of Chiba and Saino (2003) who reported that appendicularian abundance increased during the summer in the Sea of Japan. Appendicularians are eaten by fish larvae in our study area (Kodama et al., 2017a). Given that the abundance of copepods is low in the summer due to low Chl a concentrations (Chiba and Saino, 2003; Iguchi, 2004), O. longicauda may have a relatively more important role in the diets of zooplanktivorous fish during the summer than during other seasons. Microsetella and Oncaea are well known as grazers of discarded appendicularian houses (Ohtsuka and Kubo, 1991; Ohtsuka et al., 1993; Koski et al., 2007; Nishibe et al., 2015). Therefore, the increase in abundance of O. longicauda may have improved the feeding environment for Oncaea and Microsetella, resulting in increases in abundances of the two copepod taxa (Fig. 6). We can estimate the carbon flux represented by house production by O. longicauda and house ingestion by Oncaea and Microsetella. The carbon content of the discarded house (CDH) is positively correlated with size (trunk length, LT) and body carbon content (CB) of the appendicularian (Sato et al., 2003). We estimated CB of O. longicauda by the following equation in Sato et al. (2003): CB[μgind−1]=3.29×10−8LT2.85 (1) Size was not measured in our study. Therefore, for the above calculation, we assume that LT of O. longicauda was 175 μm, based on the modal values for the species (150–200 μm) obtained by Tomita et al. (1999) in the Sea of Japan during the summer. We then calculate CDH as follows (Sato et al., 2003): CDH[μ ghouse-1]=0.179×CB (2) We ignore the effects of Chl a concentration in our calculation of CDH because the Chl a concentration of Sato et al. (2003) was within the range of concentrations in our study (Fig. 2f). The product of CDH and house renewal rate (RHR) gives an estimate of the total carbon content of houses discarded on an hourly basis by an O. longicauda individual. RHR does not depend on CB, but depends on temperature and salinity in the case of O. dioica (Sato et al., 2001), and the carbon content of new houses in the case of other Oikopleura species (Sato et al., 2003). For estimating RHR, we can use the simple linear regression for the relationship between daily house renewal rate and temperature given for O. dioica in Sato et al. (2001): RHR[houses h-1]=0.9739×T-2.8361 (3) Here, we use mean water-column T as T, since the abundance of O. longicauda had a significant positive relationship with water-column T, but no relationship with SST. Although temperature varied widely in our study, salinity did not (Fig. 2); we, therefore, ignore the effect of the latter. Since the unidentified Oikopleura were significantly observed in our study, we regarded their abundances as O. longicuda in the estimation. Feeding rates of Oncaea and Microsetella can be estimated based on the literature values (Koski et al., 2007; Nishibe et al., 2015). The ingestion rate for Oncaea was calculated only for adults (after removing copepodite numbers from abundance values) as 0.3 μg C ind−1 d−1 based on Nishibe et al. (2015) results for the Kuroshio region; a rate intermediate between those in Koski et al. (2007), 0.2 μg C ind−1 d−1 and Alldredge (1972), 2.8 μg C ind−1 d−1, and the water temperature is the same level with our study. The ingestion rate for Microsetella was set as 0.02 μg C ind−1 d−1 for adults based on Koski et al. (2007) for M. norvegica. In our area, both M. norvegica and M. rosea, which is bigger than M. norvegica and attaches to discarded appendicularian houses (Steinberg et al., 1994), were present. On the basis of the assumptions and calculations above, the daily carbon content of discarded houses ranged 0–60.9 mg C m−2 d−1 (mean ± SD: 7.7 ± 7.8 mg C m−2 d−1) for O. longicauda in our study. This was within the ranges for Toyama Bay (0.11–266 mg C m−2 d−1 (Tomita et al., 1999), the Kuroshio off Honshu in early spring (7.4–8.1 mg C m−2 d−1 in the 0–150 m layer (Hidaka, 2008) and Tokyo Bay (3.6–508 mg C m−2 d−1 in the 0–25 m layer (Sato et al., 2008). The potential carbon ingestion rates for Oncaea and Microsetella were 10.6 ± 9.3 and 0.70 ± 0.55 mg C m−2 d−1, respectively. Our estimation is similar to oncaeid ingestion rates in an earlier study of the Kuroshio, 12.3–31.3 mg C m−2 d−1 (Nishibe et al., 2015). Summed carbon ingestion rates for Oncaea and Microsettela (community ingestion rate) were higher than the amount of carbon available in houses discarded daily by O. longicauda, assuming Oncaea and Microsettela feed only on discarded houses. However, this simple community ingestion rate is probably an overestimate, as Nishibe et al. (2015) reported a maximum of only 34% of Oncaea attaching to discarded houses. When factored into the community ingestion rate, this maximum percentage attachment gives a re-calculated community ingestion rate of 3.9 ± 3.3 mg C m−2 d−1, which is half of the daily amount available in house discards. At 59 of 235 stations, the community ingestion rate was estimated to be in excess of the C available through house discards. In particular, it was higher at 26 of 49 stations in 2012, and only at four stations in 2013 when the abundances of O. longicauda were significantly high. In addition, the discarded houses of O. longicauda sink 190 m d−1 (Taguchi, 1982), and Oncaea is distributed mainly at 25 m depth, and observed from 0 to 50 m depth in Toyama Bay in the Sea of Japan (Takahashi and Uchiyama, 2008). If the vertical distribution of Oncaea is assumed to be limited to a depth of <50 m, the period during which discarded houses are potentially available for ingestion is <6 h; therefore, the daily ingestion rate may remain 0.97 ± 0.82 mg C m−2 d−1, corresponding to one-eighth of the amount of C available through daily house discards. The presence of copepodites and nauplii of Oncaea provides a possible explanation of the underestimation of the community ingestion rate: the number of copepodites was higher than adults on average, and the feeding habitats of these larvae are not clear. These results suggest that zooplankton consume 12.5–100% of houses discarded daily by O. longicauda during summer in the Sea of Japan. Compared to ingestion rates for oncaeids (~10% d−1 of discarded house biomass) in other marine environments (Steinberg et al., 1997; Koski et al., 2007; Nishibe et al., 2015), our estimations are considered high, while yearly variation of our study area was observed. The strong correlations between abundances of Microsettela or Oncaea and O. longicauda may be explained by the high ingestion rates; the abundances of these two copepod species are considered to be controlled by their food supply. Interestingly, Oncaea venusta reproduce actively in warm conditions in the Sea of Japan (Hirakawa, 1995), while phytoplankton abundance is low in such waters; this may be related to the abundance of O. longicauda, which also increases in warm waters, as shown in this study. Discarded appendicularian houses are not only consumed by Oncaea and Microsettela but also by heterotrophs such as bacteria, ciliates, crustacean nauplii and polychaetes (Kiørboe, 2001). Further studies are necessary to evaluate the abundance of discarded appendicularian houses and their importance for carbon cycling in marine ecosystems, particularly in the deeper zones of the ocean, because rapid lowering of pH with increasing CO2 concentrations occurs in the deeper layers of the Sea of Japan (Chen et al., 2017). CONCLUSIONS A 5-year survey was conducted to assess the abundances of appendicularians and other zooplankton in the Sea of Japan. Ten appendicularian species were recorded. Of those, Oikopleura longicauda was the most dominant throughout the area studied. Its abundance was positively related to habitat temperature and was three times higher in 2013 than in 2014. Abundances of other appendicularians were also high in 2013. However, the reason for yearly variation is not clear in the present study. There was a positive relationship between the abundance of O. longicauda and the abundances of Microsetella and Oncaea, which feed on discarded appendicularian houses: the high abundance of O. longicauda may have positively affected these two copepod taxa. In addition, abundance of the carnivorous Sagitta was also strongly correlated with that of O. longicauda. Therefore, not only O. longicauda bodies but also their discarded houses are an important link in the transfer of energy from primary to higher trophic levels in the epipelagic ecosystem in the Sea of Japan during summer, and contribution to carbon sinking will be further studied. SUPPLEMENTARY DATA Supplementary data can be found online at Journal of Plankton Research online. ACKNOWLEDGEMENTS Samples were collected during cruises of RV Shunyo-Maru and Shoyo-Maru of the Japan Fisheries Research and Education Agency and Fisheries Agency, respectively, and we thank the captains, crews, and many researchers during the cruises. We deeply appreciate Dr K. Hidaka for providing valuable advice, Mr T. Takahashi for copepods identification and Dr S. Furukawa for advising statistics. We also acknowledge an anonymous reviewer and Dr F. Lombard for their insightful comments. FUNDING This work was financially supported by Fisheries Agency of Japan, and Japan Fisheries Research and Education Agency, and JSPS (Japan Society for the Promotion of Science) KAKENHI Grant-in-Aid for Scientific Research grant (16K07831) for T.K. REFERENCES Alldredge , A. L. ( 1972 ) Abandoned larvacean houses: a unique food source in the pelagic environment . Science , 177 , 885 – 887 . Google Scholar CrossRef Search ADS PubMed Alldredge , A. L. 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Journal of Plankton ResearchOxford University Press

Published: May 10, 2018

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