Skip to main content
NCBI home page
Zoological Studies logoLink to Zoological Studies
. 2017 May 23;56:e13. doi: 10.6620/ZS.2017.56-13

Length-weight Relationships and Chemical Composition of the Dominant Mesozooplankton Taxa/species in the Subarctic Pacific, with Special Reference to the Effect of Lipid Accumulation in Copepoda

Asami Nakamura 1,4, Kohei Matsuno 2,5, Yoshiyuki Abe 1, Hiroshi Shimada 3, Atsushi Yamaguchi 1,*
PMCID: PMC6517705  PMID: 31966212

Abstract

Asami Nakamura, Kohei Matsuno, Yoshiyuki Abe, Hiroshi Shimada, and Atsushi Yamaguchi (2017) While length-weight (L-W) regressions for warm-water zooplankton taxa from the waters neighbouring Japan already exist, they are still missing for comparable cold-water species. In this study, the L-W regressions of 41 species belonging to 12 taxa that are dominant in the Oyashio region were reported. The body length and volume of zooplankton were measured with an image-analysis system, and the effects of lipid accumulation in Copepoda on their mass and chemical composition were quantified. The L-W regressions had a high coefficient of determination (mean r2 = 0.886). For the chemical composition, the water composition ranged from 69.8 to 95.2% wet mass (WM), carbon (C) composition from 3.8 to 60.8% dry mass (DM) and nitrogen (N) composition from 1.0 to 10.1% DM. Taxon-specific differences in the chemical composition were marked for the gelatinous taxa (Appendicularia, Cnidaria, Salpida), which also had high water and low C composition. Because C is an index of lipids, high water compositions together with low lipid compositions are considered to be characteristics of the gelatinous taxa. The most significant effects of lipid accumulation in the Copepoda are changes in DM and C. Within the same developmental stage, the DM and C compositions of the full lipid-containing specimens showed 495% and 741% increases, respectively, over those of the low lipid-containing specimens. These differences exceeded the changes after moulting (78.1%) for general copepod species. Thus, lipid accumulation should be evaluated for the accurate mass estimation of boreal Copepoda by image analysis.

Keywords: Mass, L-W equation, Zooplankton, C/N, Lipids, Oil sac volume, Image analysis

BACKGROUND

In the marine ecosystem, mesozooplankton play an important role as a vital link connecting primary producers and higher trophic levels (Hunt et al. 1998; Beamish et al. 1999; Ikeda et al. 2008). The feeding preference of fishes is affected by the size of mesozooplankton (Sheldon et al. 1977), and the energy cost, growth and mortality of shes also vary with the size of mesozooplankton (van der Meeren and Næss 1993). These facts indicate that information about mesozooplankton’s size and biomass are of prime importance when evaluating energy transfer in marine ecosystems. On the other hand, mesozooplankton play an important role in the vertical material flux down to the deep layer. Mesozooplankton feed on phytoplankton, egest fast-sinking faecal pellets, and actively transport materials by the diel vertical migration (DVM), thus they have central role in the “biological pump” (Longhurst and Harrison 1989). Because the flux of the faecal pellets egested during DVM is correlated with mesozooplankton’s size and biomass (Paffenhöfer and Knowles 1979; Uye and Kaname 1994), an accurate estimation of the biomass and size of mesozooplankton is also of primary importance from the perspective of the biological pump.

The chemical composition of mesozoo- plankton varies by taxon. For instance, the Cnidaria, Appendicularia, and Salpida are known to have high water and lower organic compositions and are called “gelatinous taxa” (Larson 1986; Gorsky et al. 1988; Molina-Ramírez et al. 2015). The chemical composition is also known to vary with region and depth (e.g., geographically and vertically). For instance, the organic composition and lipid levels are higher for high-latitude species (Lee et al. 1971; Båmstedt 1986), while higher carbon and low nitrogen compositions are reported for deep-sea species (Ikeda et al. 2006). Chemical composition differences may also affect length- weight (L-W) relationships, and these relationships also vary widely by taxon and region (Uye 1982; Mizdalski 1988; Hirst 2012). Concerning the waters around Japan, information on the L-W relationships and chemical compositions of mesozooplankton is available for the warm-water regions (Uye 1982); however, little information is available for the cold- water (Oyashio) region.

In the Oyashio region, large amounts of nutrients are provided at the surface layer by strong wintertime mixing; phytoplankton form massive diatom blooms during the spring (Kasai et al. 1997). The mesozooplankton in this region is dominated by Copepoda, which utilize the spring phytoplankton bloom as energy for their growth and reproduction (Miller et al. 1984). For instance, the dominant copepods in this region, Neocalanus spp., achieve growth at the surface layer during the spring bloom, store lipids, and then migrate down to the deep layers for diapause and reproduction (Kobari and Ikeda 1999; Tsuda et al. 1999), during which the stored lipids are used for energy (Lee et al. 1970; Miller et al. 1998; Jónasdóttir 1999). Thus, the C/N ratio of copepods is known to vary seasonally and to be correlated with the amount of the lipid store (Omori 1969). While the importance of their lipid store is known, information on the effects of the lipid store of Copepoda on their L-W relationship and chemical compositions is scarce.

In this study we report the L-W relationships of various taxa (41 species belonging to 12 taxa) that are dominant in the mesozooplankton community in the Oyashio region. For the chemical composition, the water, carbon and nitrogen compositions were quantified and the differences were evaluated by separating gelatinous and semi- gelatinous taxa (Larson, 1986). For the Copepoda, the amount of stored lipid was quantified using image-analysis methods (Shimada and Oku 2014). Based on the amounts of stored lipids, the body volume, mass and chemical compositions of the Copepoda were compared and the effects of the lipid stores were evaluated for each parameter.

MATERIALS AND METHODS

Present study is a compilation of published and unpublished studies, some of which has been submitted as theses project of Hokkaido University.

Field sampling

Specimens of 41 species belonging to 12 taxa used for the L-W relationship estimation were mainly collected between the sea surface and a depth of 3000 m in the Oyashio region in the western subarctic Paci c Ocean and the adjacent northern Japan Sea (Table 1).

Zooplankton samples were collected at four stations (41°N, 145°E; 43°N, 155°E; 40°N, 155°E; 37°N, and 148°E) by vertical tows of a NORPAC net (45 cm mouth diameter, 335 μm mesh) at depths of 150 m or 500 m to the sea surface between 8 and 19 May 2015. The freshly collected samples were taken according to the procedures discussed below. Additional samples were collected by a 0-300 m vertical tow of a NORPAC net at St. O26 (45°N, 143°E) in the southern Okhotsk Sea on 5 June 2015.

Samples for analysing the effect of the lipid stores of copepods were collected for ve species: Eucalanus bungii copepodid stage six female (C6F), Metridia okhotensis C5M, C6F, Neocalanus cristatus C5, N. flemingeri C5 and C6F, and N. plumchrus C5. The specimens were sorted into three categories of lipid storage amounts (low, medium, and full) as defined by the following references: Shoden et al. (2005) for E. bungii, Padmavati et al. (2004) for M. okhotensis and Ikeda et al. (1990) for Neocalanus spp.

Table 1. Summary on mass-length regressions for various zooplankton taxa/species which dominated in the western subarctic Paci c and their adjacent seas. Note that length units are μm for meso-size taxa (Ostracoda, Copepoda and Appendicularia) and mm for the remaining macro-size taxa. For masses, units are in μg for all taxa. WM: wet mass, DM: dry mass, C: carbon, N: nitrogen, BH: bell height, TL: total length, SL: standard length, PL: prosome length, BL: body length, L: length, TrL: trunck length. Detailed diagrams of measured parts are shown in gures 1 and 2 .

Taxa Species (taxonomic category) Regression Unit r2 n p References
　 　 　 Mass Length 　 　 　 　
Cnidaria Aglantha digitale Log10DM = 1.125(Log10BH)2+1.268Log10BH+0.667 DM (μg) BH (mm) 0.976 72 Ikeda and Imamura (1996)
Other Cnidaria spp. Log10DM = 2.94Log10TL+0.82 DM (μg) TL (mm) 0.620 35 Imao (2005)
Annelida Annelida spp. Log10DM = 1.53Log10TL+1.49 DM (μg) TL (mm) 0.810 43 Imao (2005)
Ostracoda Discoconchoecia pseudodiscophora Log10DM = 2.61Log10SL-7.751 DM (μg) SL (μm) 0.992 8 Kaeriyama and Ikeda (2002)
Metaconchoecia skogsbergi Log10DM = 2.42Log10SL-7.143 DM (μg) SL (μm) 0.996 7 Kaeriyama and Ikeda (2002)
Orthoconchoecia haddoni Log10DM = 2.53Log10SL-7.511 DM (μg) SL (μm) 0.996 8 Kaeriyama and Ikeda (2002)
Copepoda Calanus pacificus (C1-C5) Log10DM = 1.871Log10PL-4.309 DM (μg) PL (μm) 0.783 21 <0.001 Ueda et al. （2008）
Log10C = 3.573Log10PL-11.008 C (μg) PL (μm) 0.857 20 <0.001 Ueda et al. （2008）
Log10N = 2.382Log10PL-7.788 N (μg) PL (μm) 0.625 13 <0.01 Ueda et al. （2008）
Eucalanus bungii (C1-C5) Log10DM = 2.052Log10PL-5.408 DM (μg) PL (μm) 0.771 93 <0.001 Ueda et al. （2008）
Log10C = 2.828Log10PL-8.97 C (μg) PL (μm) 0.879 92 <0.001 Ueda et al. （2008）
Log10N = 2.727Log10PL-9.63 N (μg) PL (μm) 0.788 53 <0.001 Ueda et al. （2008）
Gaetanus variabilis (C1-C6) Log10DM = 3.169Log10PL-8.317 DM (μg) PL (μm) 0.982 34 Yamaguchi and Ikeda (2000a)
Heterorhabdus tanneri (C3-C6) Log10DM = 3.530Log10PL-9.579 DM (μg) PL (μm) 0.998 20 Yamaguchi and Ikeda (2000b)
Metridia pacifica (C1-C5) Log10DM = 1.405Log10PL-2.865 DM (μg) PL (μm) 0.689 45 <0.001 Ueda et al. （2008）
Log10C = 2.967Log10PL-9.113 C (μg) PL (μm) 0.924 44 <0.001 Ueda et al. （2008）
Log10N = 2.902Log10PL-9.209 N (μg) PL (μm) 0.940 45 <0.001 Ueda et al. （2008）
Neocalanus cristatus (C1-C5) Log10DM = 2.418Log10PL-6.242 DM (μg) PL (μm) 0.890 67 <0.001 Ueda et al. （2008）
Log10C = 2.964Log10PL-8.931 C (μg) PL (μm) 0.900 67 <0.001 Ueda et al. （2008）
Log10N = 3.115Log10PL-10.288 N (μg) PL (μm) 0.893 62 <0.001 Ueda et al. （2008）
Neocalanus flemingeri (C4-C5) Log10DM = 4.954Log10PL-15.005 DM (μg) PL (μm) 0.669 15 <0.001 Ueda et al. （2008）
Log10C = 6.395Log10PL-20.449 C (μg) PL (μm) 0.681 14 <0.001 Ueda et al. （2008）
Log10N = 4.905Log10PL-16.345 N (μg) PL (μm) 0.306 14 Ueda et al. （2008）
Neocalanus plumchrus (C1-C5) Log10DM = 2.044Log10PL-4.881 DM (μg) PL (μm) 0.933 49 <0.001 Ueda et al. （2008）
Log10C = 3.237Log10PL-9.794 C (μg) PL (μm) 0.957 49 <0.001 Ueda et al. （2008）
Log10N = 2.235Log10PL-7.043 N (μg) PL (μm) 0.874 49 <0.001 Ueda et al. （2008）
Paraeuchaeta birostrata (Egg-C6) Log10DM = 2.882Log10PL-7.252 DM (μg) PL (μm) 0.991 ## Yamaguchi and Ikeda (2002)
Paraeuchaeta elongata (Egg-C6) Log10DM = 3.167Log10PL-8.358 DM (μg) PL (μm) 0.975 ## Yamaguchi and Ikeda (2002)
Paraeuchaeta rubra (Egg-C6) Log10DM = 2.854Log10PL-7.1102 DM (μg) PL (μm) 0.984 ## Yamaguchi and Ikeda (2002)
Pleuromamma scutullata (C1-C6) Log10DM = 2.723Log10PL-6.892 DM (μg) PL (μm) 0.995 28 Yamaguchi and Ikeda (2000b)
Pseudocalanus newmani (N2-N6) Log10DM = 2.515Log10TL-6.57 DM (μg) TL (μm) 0.951 5 Lee et al. (2003)
Pseudocalanus newmani (C1-C5) Log10DM = 2.08Log10TL-5.456 DM (μg) TL (μm) 0.988 9 Lee et al. (2003)
Scolecithricella minor (C2-C6) Log10DM = 3.669Log10PL-9.739 DM (μg) PL (μm) 0.989 22 Yamaguchi (1999)
Cyclopoid Copepoda (3 species, C1-C6) Log10DM = 1.997Log10PL-5.3245 DM (μg) PL (μm) 0.755 56 Kaneko (2005)
Poecilostomatoid Copepoda (12 species, C5-C6) Log10DM = 2.875Log10PL-7.458 DM (μg) PL (μm) 0.976 24 <0.0001 Nishibe (2005)
Other Copepoda spp. Log10DM = 2.62Log10TL-6.40 DM (μg) TL (μm) 0.670 ## Imao (2005)
Mysidacea Meterythrops microphtalma Log10DM = 3.10Log10BL+0.26 DM (μg) BL (mm) 0.987 46 Ikeda (1992)
Amphipoda Cyphocaris challengeri Log10DM = 2.83Log10BL+0.69 DM (μg) BL (mm) 0.992 17 <0.0001 Yamada (2002)
Primno abyssalis Log10DM = 2.71Log10BL+0.76 DM (μg) BL (mm) 0.992 22 <0.0001 Yamada et al. (2002)
Themisto japonica Log10DM = 2.12Log10BL+1.11 DM (μg) BL (mm) 0.912 30 <0.0001 Yamada (2002)
Themisto pacifica Log10DM = 2.72Log10BL+0.690 DM (μg) BL (mm) 0.992 21 <0.0001 Yamada (2002)
Euphausiacea Euphausia pacifica (Furcilia-Adult) Log10WM = 3.130Log10BL+0.914 WM (μg) BL (mm) 0.990 67 <0.01 Kim (2009)
Thysanoessa inspinata (Furcilia-Adult) Log10WM = 3.190Log10BL+1.041 WM (μg) BL (mm) 0.988 53 <0.01 Kim (2009)
Thysanoessa longipes (Furcilia-Adult) Log10WM = 3.263Log10BL+0.929 WM (μg) BL (mm) 0.992 55 <0.01 Kim (2009)
Chaetognatha Eukrohnia fowleri Log10DM = 3.32Log10TL-1.14 DM (μg) TL (mm) 0.950 85 Imao (2005)
Sagitta elegans Log10DM = 2.91Log10TL-0.79 DM (μg) TL (mm) 0.970 54 Imao (2005)
Other Chaetognatha spp. Log10DM = 2.80Log10TL-0.6 DM (μg) TL (mm) 0.900 96 Imao (2005)
Doliolida Dolioletta toritonis (nurse) Log10WM = 2.16Log10L+1.56 WM (μg) L (mm) 0.915 20 Aono (1999)
Dolioletta toritonis (phorozooid) Log10WM = 2.24Log10L+1.77 WM (μg) L (mm) 0.895 7 Aono (1999)
Dolioletta toritonis (gonozooid) Log10WM = 2.39Log10L+1.66 WM (μg) L (mm) 0.934 23 Aono (1999)
Salpida Cyclosalpa bakeri Log10DM = 3.03Log10L+0.2 DM (μg) L (mm) 0.968 14 Aono (1999)
Salpa aspera Log10DM = 3.66Log10L-0.74 DM (μg) L (mm) 0.963 25 Aono (1999)
Salpa fusiformis Log10DM = 2.73Log10L+0.36 DM (μg) L (mm) 0.947 24 Aono (1999)
Thalia democratica (solitary zooid) Log10DM = 2.26Log10L+0.86 DM (μg) L (mm) 0.839 19 Aono (1999)
Thalia democratica (aggregate zooid) Log10DM = 2.86Log10L+0.53 DM (μg) L (mm) 0.939 25 Aono (1999)
Appendicularia Oikopleura longicauda Log10DM = 1.988Log10TL-4.264 DM (μg) TrL (μm) 0.982 29 <0.001 Shichinohe (2000)
Mollusca Mollusca spp. Log10DM = 1.13Log10TL+2.29 DM (μg) TL (mm) 0.440 9 Imao (2005)
Open in a new tab

Mass and chemical composition measurements

Fresh specimens/samples were removed from seawater, placed on a 100-μm mesh and then rinsed briefly with distilled water to remove salt. Samples on the mesh were then placed on clean dry tissues to remove water. The water- free samples were then placed in a pre-weighed aluminium pan and frozen at -20°C. In a laboratory on land, the wet mass (WM) was measured using a microbalance (Mettler Toledo MT5) with a precision of 1 μg, and the sample was freeze-dried for ve hours and stored in a drying oven at 60°C for twelve hours. After cooling in a desiccator for several hours, the dry mass (DM) was measured with a microbalance. The water compositions (% of WM) were calculated according to the di erences in masses (water = 100 (WM - DM)/WM). The dried samples were ground, weighed, and placed in a tin cup, after which carbon (C) and nitrogen (N) were measured by a CHN coder (Vrio EL III). The C and N compositions were expressed as a percentage of the DM.

Body length and volume measurements

The measurements of the lengths of the body parts of the various taxa treated in this study are shown in figure 1. The bell height (BH) of the Cnidaria, total length (TL) of the Annelida, standard length (SL) of the Ostracoda, body length (BL) of the Mysidacea, body length (BL) of the Amphipoda, body length (BL) of the Euphausiacea, total length (TL) of the Chaetognatha, length (L) of the Doliolida, length (L) of the Salpida, trunk length (TrL) of the Appendicularia, and total length (TL) of the Mollusca were measured.

For the Copepoda, only the prosome length (PL) was measured for all of the species (Fig. 2A). The lipid stores were quantified for five species (see later), and image analyses from the dorsal and lateral views were performed using the equipment of Shimada and Oku (2014). The length (L) and width (W) of the prosome (PL and PW), urosome (UL and UW) and oil sac (OSL and OSW) were measured to a precision of 1 μm with the aid of Image J software (Figs. 2A, B). The volumes (V: mm3 ind.-1) of the prosome (PV), urosome (UV) and oil sac (OSV) were calculated with the following equation (Escribano and McLaren 1992): V = 1/6 × L × π × (W/2)2.

The total volume (TV) was calculated as the sum of the PV and UV (TV = PV + UV). To evaluate the effect of the viewing direction (dorsal and lateral views) on the volume value, we compared the volumes from both the dorsal (VD) and lateral (VL) views.

Fig. 1.

Fig. 1.

Open in a new tab

Fig. 1. Illustration showing the length measurements of various zooplankton taxa. A: bell height (BH) of Cnidaria, B: total length (TL) of Annelida, C: standard length (SL) of Ostracoda, D: body length (BL) of Mysidacea, E: body length (BL) of Amphipoda, F: body length (BL) of Euphausiacea, G: total length (TL) of Chaetognatha, H: length (L) of Doliolida, I: length (L) of Salpida, J: trunk length (TrL) of Appendicularia, K: total length (TL) of Mollusca. Note that the length measurements for Copepoda are summarized in figure 2.

Length-weight equation and analysis

To express the L-W relationship, we applied the power-law equation, which was also used by Uye (1982) for the warm-water region of Japan: Log10M = a × Log10L + b, where a and b are fitted constants, M is the mass in μg and L is the length in μm for mesozooplankton (Ostracoda, Copepoda and Appendicularia) and in mm for macrozooplankton taxa (Uye 1982). For the cnidarian Aglantha digitale, we applied an expression in a quadratic equation based on the literature (Ikeda and Imamura 1996). Most of the L-W relationships were unpublished data in theses submitted to Hokkaido University.

To evaluate the changes in the volume and mass together with the lipid store (from low to medium and full lipid), we calculated the “percentage change” index according to Hopkins et al. (1984) for E. bungii C6F, M. okhotensis C6F and N. cristatus C5. This value means that the percentage changes in the volume and mass from the values at low lipid store are expressed as 100%: Percent change = 100 × ([Full or Medium] - [Low]) / Low, where Full, Medium, and Low indicate the values at full, medium and low lipid levels, respectively (Hopkins et al. 1984). The percentage changes were calculated for volumes (PV, OSV and TV), masses (μg WM and μg DM), and chemical compositions (μg Water, μg C and μg N); the effects of lipid storage on the volume, mass, and chemical compositions were then evaluated.

Fig. 2.

Fig. 2.

Open in a new tab

Fig. 2. Diagrams of the length and volume measurements of Copepoda (Eucalanus bungii C6F with full lipid) in dorsal (A) and lateral (B) views. C: E. bungii C6F with low lipid, D: Neocalanus cristatus C5 with full lipid (left) and low lipid (right), E: Metridia okhotensis C5F with full lipid (left) and low lipid (right). PL: prosome length, PW: prosome width, OSL: oil sac length, OSW: oil sac width, UL: urosome length, UW: urosome width.

RESULTS

Length-weight equations and chemical compositions

The L-W equations of 41 species belonging to 12 taxa are summarized in table 1. For the Euphausiacea and Doliolida, the mass units were in WM and were in DM for the other taxa. For five species of Copepoda (Calanus pacificus, E. bungii, Metridia paci ca, N. cristatus, N. emingeri and N. plumchrus), the units of C and N are also shown as presented in Ueda et al. (2008). The coefficient of determination (r2) ranged between 0.306 and 0.998, and the mean value was 0.886 ± 0.145 (mean ± 1 SD).

The water, C, and N compositions of each taxon are summarized in table 2. The water compositions ranged between 69.8% WM (Thysanoessa longipes) and 95.2 ± 0.5%WM (Aglantha digitale). The C compositions ranged from 3.8 ± 4.3% DM (various cnidarian species) to 60.8 ± 3.1% DM (Paraeuchaeta rubra). The N compositions were observed between 1.0 ± 0.03% DM (Salpa fusiformis) and 10.1 ± 1.1% DM (Gaetanus variabilis).

The relationships among water, C, and N compositions are shown with scatter plots (Fig. 3). When comparing the water and C compositions, a significant negative correlation (high C composition implying low water composition) was detected for the non-gelatinous taxa (p < 0.01, Fig. 3A). The gelatinous taxa plotted at positions of high water and low C compositions. The plots of the semi- gelatinous taxa appear between the other two types of taxa. The comparison between the N and water compositions showed no correlation among them (Fig. 3B). The comparison between the C and N compositions were positively correlated in both gelatinous and non-gelatinous taxa (p < 0.0001, Fig. 3C).

Table 2. Summary on water composition (% of wet mass, %WM), carbon (C) and nitrogen (N) composition (% of dry mass, %DM) for various zooplankton taxa/species which dominated in the western subarctic Paci c and their adjacent seas. Values are mean ± 1 SD.

Taxa Species (taxinomic category) Water (%WM) C (%DM) N (%DM) References
Cnidaria Aglantha digitale 95.2±0.5 15.4±1.6 4.3±0.4 Ikeda (2014a)
Other Cnidaria spp. 3.8±4.3 1.0±1.4 This study
Annelida Annelida spp. 85.2±1.15 32.8±4.28 7.9±0.71 This study
Ostracoda Discoconchoecia pseudodiscophora 75.9 50.8±4.7 7.8±0.8 Ikeda (1990), Kaeriyama and Ikeda (2004)
Metaconchoecia skogsbergi 39.8±1.6 9.4±0.5 Kaeriyama and Ikeda (2004)
Orthoconchoecia haddoni 44 8.95 Kaeriyama and Ikeda (2004)
Copepoda Calanus pacificus (C1-C5) 18.9±13.4 3.0±2.3 Ueda et al. （2008）
Eucalanus bungii (C1-C5) 92.8±1.5 15.1±5.8 1.5±0.7 Shoden (2000), Ueda et al. （2008）
Gaetanus variabilis (C5-C6) 79.7±3.5 47.1±4.9 10.1±1.1 Ikeda et al. (2006)
Heterorhabdus tanneri (C6) 88.1 43.2 9.4 Ikeda et al. (2006)
Metridia pacifica (C1-C5) 8.0±5.3 1.5±0.8 Ueda et al. （2008）
Neocalanus cristatus (C1-C5) 83.9±8.5 30.9±20.5 3.8±2.3 Kobari et al. (2003), Ueda et al. （2008）
Neocalanus flemingeri (C4-C5) 81.6±6.3 47.8±11.6 4.5±1.8 Kobari et al. (2003), Ueda et al. （2008）
Neocalanus plumchrus (C1-C5) 86.9±4.5 22.2±15.0 4.5±2.1 Kobari et al. (2003), Ueda et al. （2008）
Paraeuchaeta birostrata (C5-C6) 70.7±4.1 58.8±2.2 7.5±0.5 Ikeda et al. (2006)
Paraeuchaeta elongata (C4-C6) 75.0±5.0 56.5±2.8 7.9±0.9 Ikeda et al. (2006)
Paraeuchaeta rubra (C5-C6) 69.9±2.6 60.8±3.1 7.5±0.6 Ikeda et al. (2006)
Pleuromamma scutullata (C6) 80.3 47.7 9.6 Ikeda et al. (2006)
Pseudocalanus newmani (C6) 47.9±5.3 9.7±1.3 Lee et al. (2001)
Scolecithricella minor (C4-C6) 80.9±2.3 Yamaguchi (1999)
Cyclopoid Copepoda (3 species) 81.4±5.1 44.8±5.9 9.8±1.8 Ikeda (2014b)
Poecilostomatoid Copepoda (12 species, C6) 52.9±5.3 8.5±1.3 Nishibe and Ikeda (2008)
Other Copepoda spp. 81.4±5.1 51.6±7.5 9.8±1.8 Imao (2005), Ikeda (2014b)
Mysidacea Meterythrops microphtalma 84.8±1.7 46.1±8.0 8.6±1.9 Ikeda (1992), Ikeda (2013b)
Amphipoda Cyphocaris challengeri 80.1±4.7 36.8±4.8 6.8±0.9 Yamada and Ikeda (2003)
Primno abyssalis 77.4±4.2 54.3±5.4 7.6±0.3 Yamada and Ikeda (2003)
Themisto japonica 77.7±2.6 46.3±2.3 8.8±0.5 Yamada and Ikeda (2003)
Themisto pacifica 77.2±2.8 47.9±7.2 8.3±1.1 Yamada and Ikeda (2003)
Euphausiacea Euphausia pacifica (Adult) 76.8±0.9 34.5±1.7 9.3±0.2 Kim (2009)
Thysanoessa inspinata (Adult) 77.2±1.6 36.3±1.0 9.8±0.3 Kim (2009)
Thysanoessa longipes (Juvenile-Adult) 69.8 41.0±9.8 8.6 Iguchi and Ikeda (2005)
Chaetognatha Eukrohnia fowleri 90.3±1.5 41.1±10.3 8.5 Imao (2005), Ikeda and Takahashi (2012)
Sagitta elegans 91.0±0.2 44.2±4.5 12.1 Imao (2005), Ikeda and Takahashi (2012)
Other Chaetognatha spp. 89.6±2.5 39.5±5.3 9.9±2.0 Imao (2005), Ikeda and Takahashi (2012)
Doliolida Dolioletta toritonis
Salpida Salpa fusiformis 4.6±0.2 1.0±0.03 This study
Appendicularia Oikopleura longicauda 29.5±2.9 7.3±2.0 Shichinohe (2000)
Mollusca Mollusca spp. 80.2±7.7 28.0±0.9 5.2±2.6 Imao (2005), Ikeda (2014b)
Open in a new tab

Fig. 3.

Fig. 3.

Open in a new tab

Fig. 3. Scatter plots of the water (water, % wet mass [WM]), carbon (C, % dry mass [DM]) and nitrogen (N, % DM) compositions for various zooplankton taxa (cf. Table 2). Plotted areas for the gelatinous taxa (Annelida, Appendicularia, Chaetognatha, Cnidaria, Mollusca and Salpida) are indicated by dashed circles. For taxa other than the gelatinous taxa, regression lines are calculated for each panel. The separation of gelatinous and semi-gelatinous taxa was derived from Larson (1986).

Effect of lipid storage in Copepoda

The mean values of the body volumes (PV, OSV, and TV), masses (WM and DM) and chemical compositions (water, C, and N) of the Copepoda were summarized for the three lipid- accumulation categories (low, medium, and full) (Table 3). Lateral (VL) view body volumes were smaller than the dorsal view (VD) values (Table 3). From a regression analysis between VL and VD in the form of VL =a×VD, where a is afitted constant, highly significant correlations were observed for all volume units (p < 0.0001) (Fig. 4). The slopes (a) of the regressions ranged between 0.538 and 0.896. Based on the mean slope values, the volume values from the lateral view (VL) were 82.1 ± 5.4% of the dorsal view (VD) for PV, 82.4 ± 5.5% for TV and 70.0 ± 12.6% for OSV (Fig. 4).

By applying the “percent change” of Hopkins et al. (1984), we analysed the volume and mass changes along with the lipid accumulation (Fig. 5). Within the treated units, the value increases were prominent, especially for OSV, DM, and C (Fig. 5). For OSV, the percent changes of the values for the medium and full lipids were 550% and 3212% of the values for the low lipids, respectively (Fig. 5). These observed values indicate a 5-fold and 32-fold OSV increase from the low-lipid accumulation to specimens with medium and full lipid accumulations, respectively. The maximum percentage change was 495% and 741% for DM and C, respectively. Species-specific differences were also detected; thus, small increases of volume and mass along with a change in lipids were observed for E. bungii C6F, while the greatest increases were observed for N. cristatus C5; the M. okhotensis C6F values were between those of these two species (Fig. 5).

The proportion of OSV to TV was standardized by calculating OSV/TV, and correlation analyses were then performed on the chemical compositions (water, C and N) (Fig. 6). With increasing OSV/TV, the water compositions decreased (r2 = 0.85, p < 0.0001, Fig. 6A), while the C compositions increased (r2 = 0.64, p < 0.001, Fig. 6B). For the N compositions, no correlations were observed for OSV/TV (Fig. 6C).

DISCUSSION

Length-weight Equation

Throughout this study, species-specific differences in L-W equations were noted, even within the same taxa. For the Copepoda, the body sizes of Paraeuchaeta spp., Neocalanus spp. and E. bungii were similar, but marked differences in mass were observed. Thus, for the same body size (PL = 3 mm), the DM values of Neocalanus spp. and Paraeuchaeta spp. were 3 or 12 times greater than that of E. bungii (Fig. 7). These species- specific differences in mass may be caused by their species-specific differences in chemical composition. Flint et al. (1991) revealed that the lipid and protein compositions of Eucalanus spp. were extremely low, 1/7-1/10 (lipid) and 1/5-1/20 (protein), respectively, of those in Calanus spp., which are called “jelly-bodied copepods” because of their low organic and high water compositions. The water composition of E. bungii evaluated in this study (92.8 ± 1.5%) (Table 2) was similar to those of the gelatinous zooplankton (i.e., > 95%, Alldredge and Madin 1982). According to Ohman (1997), the water compositions of three sympatric copepods (Rhincalanus nasutus, C. pacificus and M. pacifica) (82.3-84.3%) differed significantly from those of Eucalanus californicus (92.9%). These facts suggest that the chemical compositions of Eucalanus spp. may be similar to those of previously reported gelatinous zooplankton taxa.

The C and N compositions of E. bungii were 15.1% and 1.5% DM, respectively; those of Neocalanus spp. were 22.2-47.8% and 3.8- 4.5% DM respectively; and those of Paraeuchaeta spp. were 56.5-60.8% and 7.7-7.9% DM (Table 2), respectively. Paraeuchaeta spp., the heaviest DM species with the same body size, had high C and N compositions, while both the C and N compositions were the lowest for the lightest, E. bungii, and all of the values of Neocalanus spp. were intermediate between these two species. For zooplankton, C and N are the lipid and protein indices, respectively (Postel et al. 2000). The low C and N compositions of E. bungii suggest that individuals of this species have low lipid and protein compositions in their bodies. Because of the low organic compositions (lipid and protein), E. bungii show high water compositions as well as a transparent body colour and structure, which may function to reduce predation pressure by visual predator fishes.

From the viewpoint of feeding modes, Paraeuchaeta spp. are categorized as carnivores (Yen 1983), while Eucalanus spp. mainly feed on phytoplankton (Ohtsuka et al. 1993), and Neocalanus spp. are suspension feeders (Dagg 1993; Gi ord 1993). For carnivorous Paraeuchaeta spp., high protein compositions may provide a high swimming ability, which allows them to capture prey. For herbivorous Eucalanus spp., a high swimming ability may not be required; thus, low protein and low organic compositions (= light DM) are characteristic of this species. For the chemical compositions of Copepoda from a water column of 0 to 5000 m, a rapid decrease in the N compositions with increasing depth is explained by freedom from visual predators in the deep-water layers, allowing them to have a low swimming ability and thus low organic and protein compositions (Ikeda et al. 2006).

In this study, the low C composition of E. bungii suggests that this species stores lower amounts of lipids in their bodies. According to Larson (1986), high water and low organic compositions in zooplankton function to substantially reduce metabolism. These facts suggest that the metabolic demand of E. bungii may be low and the low lipid (C) compositions of this species may be sufficient. While E. bungii have a diapause phase in their life cycle, a mass- balance estimation between metabolic demand and lipid stores showed that the stored lipids of E. bungii are sufficient to maintain their population during the resting phase in the deep layer (Shoden et al. 2005).

As we show in this study, even the L-W equations within the same taxa showed large species-specific differences, which are related to the feeding mode, life cycle, and habitat depths of each species. The chemical compositions of marine zooplankton vary greatly with the taxa, which may be caused not only by the internal state (developmental stage, sex and nutritional condition) but also by the external conditions (season, region, geography and depth) (Omori 1969; Ikeda 1974; Båmstedt 1986). For instance, other than the Copepoda, the chemical compositions of the Amphipoda are known to be lower in C and higher in water compositions with increasing habitat depth (Ikeda 2013a). To make an exact biomass estimation, application of the general L-W equation to all taxa is not adequate. Differences between species should be considered.

Table 3. Comparison on body volume, mass and chemical composition of Copepoda (Eucalanus bungii, Metridia okhotensis, Neocalanus cristatus, Neocalanus emingeri and Neocalanus plumchrus) between full, medium and low lipid contents.

　 　 　 Volume (mm3 ind.-1) 　 Mass (mg ind.-1) 　 Chemical Composition
Species Lipid Stage (n) PVL PVD OSVL OSVD TVL TVD 　 (n) WM DM 　 (n) Water (%WM) (n) C (%DM) N (%DM)
E. bungii Full C6F 7 10.504 12.760 0.210 0.330 10.559 12.809 5 12.399 1.158 5 90.48 3 34.27 7.057
Medium C6F 9 9.413 11.199 0.034 0.036 9.463 11.247 5 11.152 0.768 5 93.09 2 28.60 7.730
Low C6F 1 11.028 10.145 0.000 0.000 11.087 10.202 2 11.501 0.861 2 92.49 1 28.00 6.470
M. okhotensis Full C5M 5 1.110 1.274 0.247 0.288 1.140 1.308 6 1.167 0.370 6 68.22 2 54.20 6.725
Full C6F 2 2.195 2.069 0.407 0.388 2.271 2.153 2 2.738 0.665 2 75.72 2 46.35 6.080
Medium C6F 6 2.259 2.592 0.052 0.104 2.354 2.685 15 2.760 0.548 15 80.14 6 43.83 8.685
Low C6F 2 2.011 2.214 0.012 0.012 2.095 2.290 2 2.720 0.393 2 85.47 1 37.40 10.220
N. cristatus Full C5 6 18.553 22.383 2.944 2.488 18.795 22.623 25 22.989 6.047 25 73.74 15 54.65 6.942
Medium C5 16 12.929 17.381 0.398 0.497 13.135 17.579 35 17.394 1.927 35 89.24 14 39.91 8.061
Low C5 6 7.114 11.337 0.226 0.292 7.243 11.459 11 11.059 1.016 11 90.91 6 38.63 9.740
N. flemingeri Full C5 9 4.110 4.678 1.333 1.826 4.157 4.719 9 5.418 1.959 9 66.69 11 51.86 7.445
Full C6F 2 7.521 9.219 2.141 2.013 7.632 9.345 1 11.093 3.813 1 65.63 1 60.40 5.900
Medium C5 10 3.168 3.676 0.478 1.012 3.213 3.719 26 3.963 1.171 26 71.11 18 53.04 7.472
Low C6F 1 4.791 7.521 0.000 0.000 4.907 7.657 1 5.963 0.334 1 94.39 1 18.50 2.610
N. plumchrus Medium C5 12 2.103 2.672 0.138 0.134 2.134 2.705 　 6 2.663 0.420 　 6 84.95 2 43.90 7.365
Open in a new tab

PV: prosome volume, OSV: oil sac volume, TV: total volume (= PV + urosome volume [UV]), WM: wet mass, DM: dry mass, Water: water content, C: carbon content, N: nitrogen content. Lower letters in volume indicate observed direction: i.e., L: lateral and D: dorsal views. (n): observed number.

Fig. 4.

Fig. 4.

Open in a new tab

Fig. 4. Comparison of volumes (prosome volume: PV, total volume: TV, oil sac volume: OSV) of five copepod species between those in lateral views (Y-axis) and dorsal views (X-axis). Positions of 1:1 are shown with dashed lines. All regressions were signi cant (p < 0.0001).

Fig. 5.

Fig. 5.

Open in a new tab

Fig. 5. Percent changes in the volumes, masses and chemical compositions of Eucalanus bungii C6F, Metridia okhotensis C6F and Neocalanus cristatus C5 along with relative lipid contents (low: L, medium: M and full: F) (cf. Table 3). PV: prosome volume, OSV: oil sac volume, TV: total volume (= PV + urosome volume [UV]), WM: wet mass, DM: dry mass, C: carbon, N: nitrogen. For volumes, the mean values of the lateral and dorsal views were applied for these calculations.

Fig. 6.

Fig. 6.

Open in a new tab

Fig. 6. Relationships between the chemical compositions (water composition: water in % wet mass (WM), carbon composition: C in % dry mass (DM) and nitrogen composition: N in % DM) and relative composition of the oil sac volume (OSV) to the total volume (TV) for various Copepoda in the subarctic Pacific Ocean (cf. Table 3). For significant relationships, regressions were calculated; ***: p < 0.001, ****: p < 0.0001, ns: not significant. The values for volume were the applied mean values of the lateral and dorsal views.

Fig. 7.

Fig. 7.

Open in a new tab

Fig. 7. Comparison of the dry mass (DM) - prosome length (PL) regressions of Copepoda of similar body sizes belonging to three genera (Paraeuchaeta, Neocalanus and Eucalanus bungii). For details of the regressions, see table 1.

Chemical compositions

For the chemical compositions of the zooplankton, noticeable differences exist between the gelatinous taxa and other taxa. In this study, we divided the zooplankton taxa into three categories according to Larson (1986). Thus, the gelatinous taxa include the Appendicularia, Cnidaria and Salpida; the non-gelatinous taxa contain the Amphipoda, Copepoda, Euphausiacea, Mysidacea and Ostracoda; and the remaining taxa, the Annelida, Chaetognatha and Mollusca, are categorized as semi-gelatinous (Larson 1986). The water compositions were 95.2% WM for the gelatinous taxa, 85.2-90.3% WM for the semi- gelatinous taxa and 69.8-86.9% WM (except for E. bungii, as previously mentioned) for the other taxa (Table 2). It should be noted that the water composition of E. bungii was extremely high (92.8% WM) as previously noted.

Proteins contain C and N at 51.3% and 17.8% DM, respectively, while for lipids, C and N constitute 69% and 0.6% DM, respectively (Rogers 1927). On the basis of these differences in the chemical compositions between protein and lipids, C is treated as an index of lipids and N as an index of the amount of protein (Postel et al. 2000). A negative correlation between the C and water compositions suggests that high lipid-containing specimens (= high C composition) may contain relatively less water as a percent of body volume. This pattern (inverse relationship between C and water composition) is reported for fishes and crustaceans (Love 1970; Ikeda et al. 2004).

The comparison of N and water composition showed no correlation between them (Fig. 3B). The gelatinous taxa were plotted at a high water composition, while the semi-gelatinous taxa were plotted at similar positions to those of the other taxa, and fewer taxonomic differences were detected for the N compositions (Fig. 3B). The amount of protein may thus have little effect on the water composition, and the DM protein compositions show little difference between the gelatinous and non-gelatinous taxa.

Both the gelatinous and non-gelatinous taxa showed positive correlations between the C and N compositions (p < 0.0001, Fig. 3C). Compared with the non-gelatinous taxa, the gelatinous taxa were characterized by low C, while both taxa had similar N composition. The high water composition of the gelatinous taxa may reduce the relative levels of C (= lipid), while they had less effect on the N compositions (= protein).

Bailey et al. (1995) noted that gelatinous taxa are characterized by high water and ash and low C and N compositions. As a function of a lower organic composition of their bodies, reduced metabolism and faster growth rates are reported (Larson 1986). With regard to the feeding mode, the gelatinous zooplankton are divided into two categories, filter feeders (i.e., Salpida and Doliolida) and carnivores (Cnidaria). The relationship between the WM and CM is reported to vary with the feeding mode; specifically, exponential increases for filter feeders and linear increases for carnivores (Molina-Ramírez et al. 2015). The rapid increase in WM with increasing CM for filter feeders may serve to increase the surface area and increase the food-capture surfaces (Molina-Ramírez et al. 2015). For the Cnidaria, chemical composition varies according to the body part (Larson 1986). These facts suggest that the chemical compositions exhibit large variability and diversity for the taxa/species within the gelatinous taxa.

Effect of lipid accumulation in Copepoda

In all copepods, the volumes (PV, OSV, and TV) observed from the dorsal view (VD) were greater than those observed from the lateral view (VL) (Fig. 4). This indicates that the proportions of the copepod prosome and urosome, as well as their oil sacs, are dorsally flattened shapes. Using an image-analysis system, Miller et al. (2000) quantified the OSV of the copepod Calanus finmarchicus from both the dorsal and lateral views and reported that the VD was greater than the VL, which corresponded with the results of this study.

For copepod species in general, the percentage change in the individual DM as a result of one moulting ranged from 61.7 to 94.0% (78.1 ± 13.7% [mean ± 1 SD]) (Mauchline 1998). In this study, the DM within the same copepodid stage showed changes of 495% depending on the amount of lipid accumulation (N. cristatus C5, Table 3). These differences in the DM are much higher than those of the copepodid moulting stage. To accurately estimate the DM of Copepoda from L-W relationships, the effect of lipid accumulation should be considered.

The C:N ratio is known to be an index of lipid accumulation (Postel et al. 2000). Omori (1969) reported that the C:N ratio of Calanus cristatus (= N. cristatus) had a maximum in May and a minimum in December, with a twofold seasonal difference in the C:N ratio. Similar seasonal changes were also reported for C. plumchrus (= N. plumchrus) and M. okhotensis (Omori 1969). The amount of food availability is also known to be a critical factor for determining lipid accumulation (Escribano and McLaren 1992).

Acknowledgments

Acknowledgments: We thank the captains, officers and crew of the T/S Oshoro-Maru of Hokkaido University and the R/V Hokuyo-Maru of the Hokkaido Research Organization. Most of the L-W equations summarized in this study are derived from various studies in the Plankton Laboratory of Hokkaido University under the supervision of Emer. Prof. Tsutomu Ikeda. Part of this study was supported by Grant-in-Aid for Scientific Research 17H01483 (A), 16H02947 (B) and 15KK0268 (Joint International Research) from the Japanese Society for Promotion of Science (JSPS). This work was partially conducted for the Arctic Challenge for Sustainability (ArCS) project.

References

  1. Alldredge A L, Madin L P. Pelagic tunicates: unique herbivores in the marine plankton. BioScience. 32:655–663. [Google Scholar]
  2. Aono T. Latitudinal distribution and annual changes of Salpida and Doliolida along 180° longitude in the northern North Pacific during summer. 1999.
  3. Bailey T G, Youngbluth M J, Owen G P. Chemical composition and metabolic rates of gelatinous zooplankton from midwater and benthic boundary layer environments off Cape Hatteras. Mar Ecol Prog Ser. 122:121–134. [Google Scholar]
  4. Båmstedt U. Chemical composition and energy content. Clarendon Press. 0:1–58. [Google Scholar]
  5. Beamish R J, Leask K D, Ivanov O A, Balanov A A, Orlov A M, Sinclair B. The ecology, distribution and abundance of midwater fishes of the Subarctic Pacific gyres. Prog Oceanogr. 43:399–442. [Google Scholar]
  6. Dagg M. Sinking particles as a possible source of nutrition for the large calanoid copepod Neocalanus cristatus in the subarctic Pacific. Deep-Sea Res I. 40:1431–1445. [Google Scholar]
  7. Escribano R, Mclaren I A. Influence of food and temperature on lengths and weights of two marine copepods. J Exp Mar Biol Ecol. 159:77–88. [Google Scholar]
  8. Flint M V, Drits A V, Pasternak A F. Characteristic features of body composition and metabolism in some interzonal copepods. Mar Biol. 111:195–205. [Google Scholar]
  9. Gifford D J. Protozoa in the diets of Neocalanus spp. in the oceanic subarctic Pacific Ocean. Prog Oceanogr. 32:223–237. [Google Scholar]
  10. Gorsky G, Dallot S, Sardou J, Fenaux R, Carré C, Palazzoli I. C and N composition of some northwestern Mediterranean zooplankton and micronekton species. J Exp Mar Biol Ecol. 124:133–144. [Google Scholar]
  11. Hirst A G. Intraspecific scaling of mass to length in pelagic animals: Ontogenetic shape change and its implications. Limnol Oceanogr. 57:1579–1590. [Google Scholar]
  12. Hopkins Cce, Tande K S, Grønvik S, Sargent J R. Ecological investigations of the zooplankton community of Balsfjorden, Northern Norway: An analysis of growth and overwintering tactics in relation to niche and environment in Metridia longa (Lubbock), Calanus finmarchicus (Gunnerus) Thysanoessa inermis (Krøyer) and T. raschi (M. Sars. 82:77–99. [Google Scholar]
  13. Hunt G L, Russell R W, Coyle K O, Weingnartner T. Comparative foraging ecology of planktivorous auklets in relation to ocean physics and prey availability. Mar Ecol Prog Ser. 167:241–259. [Google Scholar]
  14. Iguchi N, Ikeda T. Effects of temperature on metabolism, growth and growth efficiency of Thysanoessa longipes (Crustacea: Eupahusiacea) in the Japan Sea. J Plankton Res. 27:1–10. [Google Scholar]
  15. Ikeda T. Nutritional ecology of marine zooplankton. Mem Fac Fish Hokkaido Univ. 22:1–97. [Google Scholar]
  16. Ikeda T. Ecological and biological features of a mesopelagic ostracod Conchoecia pseudodiscophora in the Japan Sea. Mar Biol. 107:453–461. [Google Scholar]
  17. Ikeda T. Growth and life history of the mesopelagic mysid Meterythrops microphthalma in the southern Japan Sea. J Plankton Res. 14:1767–1779. [Google Scholar]
  18. Ikeda T. Metabolism and chemical composition of marine pelagic amphipods: synthesis toward a global bathymetric model. J Oceanogr. 69:339–355. [Google Scholar]
  19. Ikeda T. Metabolism and chemical composition of pelagic decapod shrimps: synthesis toward a global bathymetric model. J Oceanogr. 69:671–686. [Google Scholar]
  20. Ikeda T. Synthesis toward a global model of metabolism and chemical composition of medusae and ctenophores. J Exp Mar Biol Ecol. 456:50–64. [Google Scholar]
  21. Ikeda T. Metabolism and chemical composition of marine pelagic gastropod molluscs: a synthesis. J Oceanogr. 70:289–305. [Google Scholar]
  22. Ikeda T, Imamura A. Abundance, vertical distribution and life cycle of the hydromedusa Aglantha digitale in Toyama Bay, southern Japan Sea. Bull Plankton Soc Japan. 43:1–43. [Google Scholar]
  23. Ikeda T, Takahashi T. Synthesis towards a globalbathymetric model of metabolism and chemical composition of marine pelagic chaetognaths. J Exp Mar Biol Ecol. 424:78–88. [Google Scholar]
  24. Ikeda T, Hirakawa K, Kajihara N. Some characteristics of a coldwater copepod Calanus cristatus from regions of Japan Sea covered by the Tsushima warm current. Bull Japan Sea Natl Fish Res Inst. 40:51–65. [Google Scholar]
  25. Ikeda T, Sano F, Yamaguchi A. Metabolism and body composition of a copepod (Neocalanus cristatus: Crustacea) from bathypelagic zone of the Oyashio region, western subarctic Pacific. Mar Biol. 145:1181–1190. [Google Scholar]
  26. Ikeda T, Yamaguchi A, Matsuishi T. Chemical composition and energy content of deep-sea calanoid copepods in the Western North Pacific Ocean. Deep-Sea Res I; 2006. 53 [Google Scholar]
  27. Ikeda T, Shiga N, Yamaguchi A. Structure, biomass distribution and trophodynamics of the pelagic ecosystem in the Oyashio region, western subarctic Pacific. J Oceanogr. 64:339–354. [Google Scholar]
  28. Imao F. Zooplankton community structure and functional role in carbon cycle in the Oyashio region, western North Pacific. 2005.
  29. Jónasdóttir S H. Lipid content of Calanus finmarchicus during overwintering in the Faroe-Shetland Channel. Fish Oceanogr. 8:61–72. [Google Scholar]
  30. Kaeriyama H, Ikeda T. Body allometry and developmental characteristics of the three dominant pelagic ostracods (Discoconchoecia pseudodiscophora, Orthoconchoecia haddoni, and Metaconchoecia skogsbergi) in the Oyashio region, western North Pacific. Plankton Biol Ecol. 49:97–100. [Google Scholar]
  31. Kaeriyama H, Ikeda T. Metabolism and chemical composition of mesopelagic ostracods in the western North Pacific Ocean. ICES J Mar Sci. 61:535–541. [Google Scholar]
  32. Kaneko M. Ecological studies on oithonid copepods in the western subarctic Pacific. 2005.
  33. Kasai H, Saito H, Yoshimori A, Taguchi S. Variability in timing and magnitude of spring bloom in the Oyashio region, the subarctic Pacific off Hokkaido. Japan. Fish Oceanogr. 6:118–129. [Google Scholar]
  34. Kim H S. Ecological and physiological studies of euphausiids in the Oyashio region, western subarctic Pacific. 2009.
  35. Kobari T, Ikeda T. Vertical distribution, population structure and life cycle of Neocalanus cristatus (Crustacea: Copepoda) in the Oyashio region, with notes on its regional variations. Mar Biol. 134:683–696. [Google Scholar]
  36. Kobari T, Shinada A, Tsuda A. Functional roles of interzonal migrating mesozooplankton in the western subarctic Pacific. Prog Oceanogr. 57:279–298. [Google Scholar]
  37. Larson R J. Water content, organic content, and carbon and nitrogen composition of medusae from the Northeast Pacific. J Exp Mar Biol Ecol. 99:107–120. [Google Scholar]
  38. Lee R F, Nevenzel J C, Paffenhöffer G A. Wax esters in marine copepods. Science. 167:1510–1511. doi: 10.1126/science.167.3924.1510. [DOI] [PubMed] [Google Scholar]
  39. Lee R F, Hirota J, Barnett A M. Distribution and importance of wax esters in marine copepods and other zooplankton. Deep-Sea Res. 18:1147–1165. [Google Scholar]
  40. Lee H W, Ikeda T, Ban S. Metabolism, body composition (C and N) and estimated net growth efficiency of a calanoid copepod Pseudocalanus newmani raised at different temperatures in the laboratory. Plankton Biol Ecol. 48:114–120. [Google Scholar]
  41. Lee H W, Ban S, Ikeda T, Matsuishi T. Effect of temperature on development, growth and reproduction in the marine copepod Pseudocalanus newmani at satiating food condition. J Plankton Res. 25:261–271. [Google Scholar]
  42. Longhurst A R, Harrison W G. The biological pump: Profiles of plankton production and consumption in the open ocean. Prog Oceanogr. 22:47–123. [Google Scholar]
  43. Love R M. The Chemical Biology of Fishes. London): Academic Press; 1970. [Google Scholar]
  44. Mauchline J. The biology of calanoid copepods. Adv Mar Biol. 33:1–710. [Google Scholar]
  45. Miller C B, Frost B W, Batchelder H P, Clemons M J, Conway R E. Life histories of large, grazing copepods in a subarctic ocean gyre: Neocalanus plumchrus, Neocalanus cristatus and Eucalanus bungii in the Northeast Pacific. Prog Oceanogr. 13:201–243. [Google Scholar]
  46. Miller C B, Crain J A, Morgan C A. Oil storage variability in Calanus finmarchicus. ICES J Mar Sci. 57:1786–1799. [Google Scholar]
  47. Miller C B, Morgan C A, Prahl F G, Sparrow M A. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine. Limnol Oceanogr. 43:488–497. [Google Scholar]
  48. Mizdalski E. Weight length data of zooplankton in the Weddell Sea in austral spring 1986 (ANT V/3) Ber Polarforsch. 55:1–72. [Google Scholar]
  49. Molina-Ramírez A, Cáceres C, Romeo-Romeo S, Bueno J, González-Gordillo J I, Irigoien X, Sostres J, Bode A, Mompeán C, Puelles M F, Echevarria F, Duarte C M, Acuña J L. (Poecilostomatoida) in the Oyashio region, western subarctic Pacific: its community structure, vertical distribution, life cycle and metabolism. J Plankton Res; 2015. 37 [Google Scholar]
  50. Nishibe Y, Ikeda T. Metabolism and elemental composition of four oncaeid copepods in the western subarctic Pacific. Mar Biol. 153:397–404. [Google Scholar]
  51. Ohman M D. On the determination of zooplankton lipid content and the occurrence of gelatinous copepods. J Plankton Res. 19:1235–1250. [Google Scholar]
  52. Ohtsuka S, Ohaye S, Tanimura A, Fukuchi M, Hattori H, Sasaki H, Matsuda O. Feeding ecology of copepodid stages of Eucalanus bungii on the Chukchi and Northern Bering seas in. Proc NIPR Symp Polar Biol. 6:7–37. [Google Scholar]
  53. Omori M. Weight and chemical composition of some important oceanic zooplankton in the North Pacific Ocean. Mar Biol. 3:4–10. [Google Scholar]
  54. Padmavati G, Ikeda T, Yamaguchi A. Life cycle, population structure and vertical distribution of Metridia spp. (Copepoda: Calanoida) in the Oyashio region. NW Pacific Ocean. 270:81–198. [Google Scholar]
  55. Paffenhöfer ‎, Knowles G-A. Ecological implications of fecal pellet size, production and consumption by copepods. J Mar Res. 37:35–49. [Google Scholar]
  56. Postel L, Fock H, Hagen W. Biomass and abundance. Academic Press. 0:83–192. [Google Scholar]
  57. Rogers C G. Textbook of Comparative Physiology. New York): McGraw-Hill; 1927. [Google Scholar]
  58. Sheldon R W, Whjr Sutcliffe, Paranjape M. Structure of pelagic food chain and relationship between plankton and fish production. J Fish Res Bd Can. 34:2344–2353. [Google Scholar]
  59. Shichinohe Y. Seasonal changes in community structure, vertical distribution and production of Appendicularia in the Oyashio region. 2000.
  60. Shimada H, Oku O. Zooplankton imaging and measurement using a digital single-lens reflex camera with macro lens. Bull Plankton Soc Japan. 61:87–90. [Google Scholar]
  61. Shoden S. Biological and ecological studies on planktonic copepod Eucalanus bungii Giesbrecht in the Oyashio region. 2000.
  62. Shoden S, Ikeda T, Yamaguchi A. Vertical distribution, population structure and life cycle of Eucalanus bungii (Copepoda: Calanoida) in the Oyashio region, with notes on its regional variations. Mar Biol. 146:497–511. [Google Scholar]
  63. Tsuda A, Saito H, Kasai H. Life histories of Neocalanus flemingeri and Neocalanus plumchrus (Calanoida: Copepoda) in the western subarctic Pacific. Mar Biol. 135:533–544. [Google Scholar]
  64. Ueda A, Kobari T, Steinberg D K. Body length, weight and chemical composition of ontogenetically migrating copepods in the Western Subarctic Gyre of the North Pacific Ocean. Bull Plankton Soc Japan. 55:107–114. [Google Scholar]
  65. Uye S. Length-weight relationships of important zooplankton from the Inland Sea of Japan. J Oceanogr Soc Japan. 38:149–158. [Google Scholar]
  66. Uye S, Kaname K. Relations between fecal pellet volume and body size for major zooplankters of the Inland Sea of Japan. van der Meeren T, Naess T. 1993. How does cod (Gadus morhua) cope with variability in feeding conditions during early larval stages. 50:637–647. [Google Scholar]
  67. Yamada Y. Life history, metabolism and production of four pelagic amphipods in the Oyashio region, western subarctic Pacific. Hokkaido University): 2002. [Google Scholar]
  68. Yamada Y, Ikeda T. Metabolism and chemical composition of four pelagic amphipods in the Oyashio region, western subarctic Pacific. Mar Ecol Prog Ser. 253:233–241. [Google Scholar]
  69. Yamada Y, Ikeda T, Tsuda A. Abundance, growth and life cycle of the mesopelagic amphipod Primno abyssalis (Hyperiidea: Phrosinidae) in the Oyashio region, western subarctic Pacific. Mar Biol. 141:333–341. [Google Scholar]
  70. Yamaguchi A. Life cycle of several small calanoid copepods neighboring waters of Japan. 1999.
  71. Yamaguchi A, Ikeda T. Vertical distribution, life cycle, and developmental characteristics of the mesopelagic calanoid copepod Gaidius variabilis (Aetideidae) in the Oyashio region, western North Pacific. Mar Biol. 137:99–109. [Google Scholar]
  72. Yamaguchi A, Ikeda T. Vertical distribution, life cycle and body allometry of two oceanic copepods (Pleuromamma scutulata and Heterorhabdus tanneri) in the Oyashio region, western North Pacific Ocean. J Plankton Res. 22:29–46. [Google Scholar]
  73. Yamaguchi A, Ikeda T. Reproductive and developmental characteristics of three mesopelagic Paraeuchaeta species (Copepoda: Calanoida) in the Oyashio region, western subarctic Pacific Ocean. Bull Fac Fish Hokkaido Univ. 53:11–21. [Google Scholar]
  74. Yen J. Effects of prey concentration, prey size, predator life stage, predator starvation, and season on predation rates of the carnivorous copepod Euchaeta elongata. Mar Biol. 75:69–77. [Google Scholar]

Articles from Zoological Studies are provided here courtesy of Biodiversity Research Center, Academia Sinica

RESOURCES