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Diel vertical distribution and migration of a euphausiid Euphausia pacifica in the Southern Yellow Sea
ARTICLE IN PRESS Deep-Sea Research II 57 (2010) 594–605
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Diel vertical distribution and migration of a euphausiid Euphausia pacifica in the Southern Yellow Sea Hui-Lian Liu a, Song Sun b,n a b
Department of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
a r t i c l e in f o
a b s t r a c t
Article history: Accepted 30 October 2009 Available online 11 November 2009
Stage-specific differences in the diel vertical distribution and migration of a euphausiid, Euphausia pacifica, were studied at a single station (E2, 70 m water depth) in the South Yellow Sea, by sampling with a conical closing net from five discrete strata, every 3 h, for 24 h, on 2–3 May 2001. Environmental data were collected simultaneously with the net sampling. Results showed that eggs contributed a large proportion of the numerical abundance of the Euphausia pacifica population throughout the investigation. They were mainly distributed below 20 m depth, and concentrated in the 30–50 m strata throughout the day and night. Nauplius stage I (NI) was distributed below 10 m, and seldom occurred in the upper 10 m. Nauplius stage II (NII) and Metanauplius stage (MN) extended their distribution to nearly the whole water column; however, the MN resided somewhat shallower than NII. The majority of calyptopis stages I to III (CI to CIII ) and early furcilia stages I to III (FI to FIII) were restricted to the upper 30 m throughout the day. The weighted mean depth tended to increase as the stage progressed from stage FI onward. Calyptopis stages showed a weak or moderate diel vertical migration behavior, and the onset of an obvious diel vertical migration took place in FII stage. The amplitude of the diel vertical migration varied with developmental stages. Stages after FIV were often absent from samples during the investigation, but from the limited available data, DVM occurred from stages FIV–VI and female adults. However, the male adults showed a somewhat different migration behavior. In summary, an ontogenetic migration pattern is obvious from this high-frequency sampling: spawning took place at 20–50 m depth, hatched nauplii sank a little, metanauplius began moving toward the surface, and calyptopis larvae reached the uppermost layer. Furcilia larvae began DVM and deepened their daytime residence depth with age. The vertical distribution of Euphausia pacifica seemed to relate to temperature and chlorophyll a. & 2009 Elsevier Ltd. All rights reserved.
Topical issue on ‘‘Krill Biology and Ecology.’’ The issue is compiled and guest-edited by the North Pacific Marine Science Organization (PICES), International Council for the Exploration of the Sea (ICES), and Global Ocean Ecosystem Dynamics (GLOBEC) project. Keywords: Euphausia pacifica Euphausiid Vertical distribution Diel vertical migration Yellow Sea
1. Introduction Euphausia pacifica is widely distributed in the North Pacific Ocean (Brinton, 1962; Mauchline and Fisher, 1969) and its adjacent coastal waters (Ponomareva, 1966; Ross et al., 1982; Endo, 1984; Cai, 1986; Sawamoto, 1992; Yoon et al. 2000). Off the China coast, Euphausia pacifica is commonly found in the Yellow Sea and the East China Sea (Anon., 1977; Zhang et al., 1991; Wang et al., 2003), especially in the Yellow Sea north of 341N, where this species is the dominant euphausiid species in most seasons (Huang, 1986). Many studies have been carried out on the distribution, life history and fishery of Euphausia pacifica in the past 50 years over its wide range (Nicol and Endo, 1997, Endo, 2000a, b, c). However, studies on this species in the Yellow Sea
n
Corresponding author. E-mail addresses: [email protected] (H.-L. Liu), [email protected] (S. Sun). 0967-0645/$ - see front matter & 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2009.10.009
and the East China Sea are relatively scarce, being confined to species occurrence and morphology descriptions (Hong, 1969; Cai, 1982), abundance and spatial distribution (Chen et al., 1980; Cai, 1986; Yoon et al., 2000; Wang et al., 2003; Wang and Zuo, 2004; Xu and Li, 2005), larval development (Suh et al., 1993; Liu and Sun, 2002) and gut content analysis and feeding (Kang, 1966, 1986). Diel vertical migration of juvenile and adult Euphausia pacifica is well studied (Brinton, 1967; Cooney, 1971; Frost and McCrone, 1974; Youngbluth, 1976; Terazaki et al., 1986; Bollens et al., 1992; Iguchi et al., 1993; Iguchi, 1995; Yoon et al., 2000; Taki, 2003; Nakagawa et al., 2003; Endo and Yamano, 2006), however most of these studies were focused on the post-larval stages. A few studies concerning the diel vertical migration of different stages or size classes were carried out off Japan (Iguchi, 1995; Taki, 2003) or in the north-east Pacific (Bollens et al., 1992); however, the sampling frequency in these studies was usually low. Up to now, little data were obtained on the diel vertical migration of Euphausia pacifica in the Yellow Sea, let alone studies on the DVM of separate developmental stages.
ARTICLE IN PRESS H.-L. Liu, S. Sun / Deep-Sea Research II 57 (2010) 594–605
The purpose of this paper is to present the results of a study of the stage-specific diel vertical distribution and migration of Euphausia pacifica based on high-frequency sampling at a station in the Yellow Sea in spring with a discussion of how the environmental factors might influence the DVM.
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(1993), Boden (1950) and Cai (1982). Abundances were calculated from volumes filtered (assuming 100% efficiency) as ind. m 3. For each developmental stage, the weighted mean depth (WMD) was calculated according to the equation: WMD= P P ( nidi)/ ni (Frost and Bollens, 1992), where ni is abundance 3 (ind. m ) at depth di, and di is the midpoint of each depth stratum.
2. Materials and methods 2.2. Observation of environmental factors 2.1. Sampling station, sampling protocol and sample analysis Multidisciplinary investigations were carried out during the cruises aboard the R. V. Dongfanghong No. 2 in the East China Sea and the South Yellow Sea from 30 April to 11 May, 2001. A total of seven stations were sampled: E1 (351000 N, 1211000 E, depth: 35 m), E2 (341300 N, 1231060 E, depth: 70 m), E4 (311000 N, 1221300 E, depth: 20 m), E5 (291000 N, 1221300 E, depth: 48 m), E6 (291000 N, 1251300 E, depth: 79 m), P1 (281100 N, 127147.50 E, depth: 1015 m) and P2 (281350 N, 126122.50 E, depth: 195 m). The En (n = 1, 2y) stations were fixed stations (the ship was at anchor) where a series of in situ measurements or samples were taken. E2 is a station in the area of the South Yellow Sea Cold Water Mass (SYCWM) (Zhang et al.,1996) where Euphausia pacifica often aggregate in spring (Anon., 1977). It was chosen for our diel study since, unlike the other stations, Euphausia pacifica are usually abundant here in spring and all stages of Euphausia pacifica can occur there. Zooplankton samples were collected nine times over a 24 h period using a conical closing net (mouth diameter: 0.8 m, length: 2.8 m, mesh opening: 0.32 mm) from 5 strata (0–10, 10–20, 20–30, 30–50 and 50–68 m) at 3 h intervals from 15:00 on 2 May to 15:00 on 3 May 2001 at station E2 (Fig. 1). Each time the towing operations lasted less than 25 min. The times of local sunrise and sunset were around 05:00 and 18:30, respectively. Zooplankton samples were preserved in a 5% formalin-seawater solution immediately after sampling. Each developmental stage, namely, egg, nauplius I–II (NI–II), metanauplius (MN), calyptopis I–III (CI–III), furcilia I–VI (FI–VI), juvenile, female adults and male adults of Euphausia pacifica was sorted and identified using a dissecting microscope according to the descriptions of Suh et al.
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Vertical profiles of water temperature, salinity and density were recorded with a CTD system (Sea-Bird SBE 9) down to the bottom at time intervals coinciding with the net samplings. The vertical profiles of chlorophyll a were determined from seawater samples collected at 3 h intervals coinciding with the net sampling from depths of 0, 10 or 12.5, 25, 38 or 40, 50 m, and near the bottom. Water samples (250 ml) were filtered through glass-fiber filters (Whatman GF/F), and then extracted with 90% acetone for 24 h in darkness. The concentration of chlorophyll a was measured using a Turner Designs (Model II) fluorometer calibrated with pure chlorophyll a (Sigma).
3. Results 3.1. Environmental factors Diel vertical variations in temperature at the sampling station are shown in Fig. 2A. Surface water temperature ranged from 11.7 to 12.7 1C, and bottom temperature varied between 8.8 and 9.4 1C. A thermocline of 3 1C difference (ranged from 9 to 11 1C) formed between 15 and 25 m. Intermediate Cold Water (ICW) existed at this station day and night, with a temperature inversion at the depth of about 25–30 m (Figs. 2A and 3A), which varied between 7.5 and 8.3 1C. Below 40 m, temperature was relatively uniform, ranging between 8.5 and 9.4 1C (Figs. 2A and 3A). Salinity varied between 32.31 and 33.27 in the water column during the investigation. Surface salinity ranged from 32.31 to 32.72. A salinity maximum often appeared in the upper water column at the base of the mixed layer, at depths ranging between 10–25 m (Fig. 3B). A salinity minimum (32.35–32.62) occurred at a similar depth as the corresponding temperature minimum. An indistinct halocline existed between 25–40 m (Figs. 2B and 3B). Bottom salinity ranged between 33.01 and 33.27. Chlorophyll a changed significantly from 0.2 to 5.7 mg m 3 in the water column. The chlorophyll maximum was found at 20–30 m with the highest values (2.5–5.7 mg m 3) recorded at 25 m, just under the thermocline. The concentrations above 10 m and below 35 m were usually less than 1.00 mg m 3 (Fig. 2C). Water density increased consistently from the surface to the bottom except at 24:00 h, when surface values were higher and the value at 15 m was obviously lower than the former and the latter sampling times (Fig. 2D). The vertical fine structure of temperature and salinity (Fig. 3) indicated that the upper mixed zone was not well mixed, and this suggested weak intrusions of water masses with different characteristics existed. Especially at 24:00 h, when a water mass with relatively high temperature, high salinity, low chlorophyll a and high water density (kg m 3-1000), came through the surface at the study site (Fig. 2). 3.2. Diel vertical distribution and migration
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Fig. 1. Sampling station E2 with superimposed depth contours (20, 50 and 80 m).
Eggs were more abundant than the other components (NI, NII, MN, CI, CII, CIII, FI, FII, FIII, FIV, FV, FVI, juvenile, female adults and
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Fig. 2. Diel variations in vertical profiles of temperature (1C), salinity (psu), chlorophll a (mg m 3), water density (kg m 3-1000) and Euphausia pacifica density (ind. m 3) at sampling station from 15:00, 2 May to 15:00, 3 May 2001. A. temperature, B. salinity, C. Chlorophll a, D. water density, E. eggs, F. nauplius, G. metanauplius, H. total calyptopis, I. total furcilia, J. post-larvae, K. total larvae and L. total population.
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20 40 60 80 Fig. 3. Vertical profiles of temperature (1C) and salinity (psu) at sampling station at 3 h intervals from 15:00 on 2 May to 15:00 on 3 May, 2001.
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Table 1 Contribution by % of numerical abundance of each developmental stage to the total abundance of whole Euphausia pacificaa population at each sampling time. Sampling time
Egg NI NII MN CI CII CIII FI FII FIII FIV FV FVI J Female Male
Day
Night
Day
average
15:00
18:00
21:00
24:00
03:00
06:00
09:00
12:00
15:00
63.20 1.84 1.36 5.34 14.85 8.54 2.91 1.26 0.39 0.19 0.10 0 0 0 0 0
84.59 0.05 2.62 6.12 1.26 2.13 0.55 0.87 0.66 0.87 0.16 0.11 0 0 0 0
66.81 0.74 5.25 11.24 7.77 4.31 2.00 0.53 0.11 0.53 0.53 0 0 0 0.11 0.11
69.67 0.15 2.08 2.46 6.62 6.39 6.00 2.16 2.16 1.62 0.62 0.08 0 0 0 0
41.82 0.56 1.31 3.00 11.25 22.64 13.64 3.56 0.70 0.80 0.47 0.05 0.05 0 0.05 0.09
31.97 1.87 1.83 4.91 14.90 20.86 14.86 6.33 1.46 0.54 0.25 0.08 0 0.04 0 0.08
39.31 0.47 0.76 8.59 16.59 19.04 10.28 3.33 0.93 0.53 0.12 0 0 0 0.06 0
65.08 0.02 0.30 2.41 9.54 9.56 6.76 4.30 1.29 0.54 0.16 0.02 0.02 0 0 0
53.59 0 0.18 1.37 13.18 15.81 10.34 4.56 0.63 0.35 0 0 0 0 0 0
57.34 0.64 1.74 5.05 10.66 12.14 7.48 2.99 0.92 0.66 0.27 0.04 0.01 0 0.02 0.03
-3
Abundance (ind. m ) 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200
Depth (m)
0 20 40 60 Egg
80 0
2
4
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0
2
4
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2
4
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2
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2
4
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NI
80 0
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NII
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20
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100 0
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50
100 0
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100 0
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100
0 20 40 60
CII
80
Fig. 4. Vertical distribution in numerical abundance (ind. m 3) of each developmental stage of Euphausia pacifica at 3 h intervals from 15:00, 2 May to 15:00, 3 May 2001. NI–NII: nauplius stage; MN: metanauplius stage; CI–CIII: calyptopis stage; FI–FVI: furcilia stage; J: juvenile; F: female; M: male; T: total population.
ARTICLE IN PRESS H.-L. Liu, S. Sun / Deep-Sea Research II 57 (2010) 594–605
0
30
60 0
30
60 0
30
60 0
30
60 0
30
60 0
30
60 0
599
30
60 0
30
60 0
30
60
0 20 40 CIII 60 80 0
10
20
0
10
20
0
10
20
0
10
20
0
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20
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20
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20
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Fig. 4. (Continued)
male adults), accounting for 32.0–84.6%, (mean=57.3%), of the total number of Euphausia pacifica in the water column during the investigation (Table 1). Eggs were distributed almost throughout the water column, but most commonly occurred below 20 m depth, and aggregated at 30–50 m (Fig. 4). Eggs were more abundant in the daytime than during nighttime, with the maximum abundance appearing at 12:00 (86.5 ind. m 3), and the lowest at 21:00 (18.6 ind. m 3) (Table 2). The WMDs of eggs ranged from 31.0 to 47.2 m, (mean=37.5 m), during the investigation (Fig. 5). The vertical distribution of eggs dominated the vertical distribution pattern of the whole Euphausia pacifica population at most sampling times during the investigation (Figs. 2E and 4). NI contributed only a small portion, 0–1.9%, (mean= 0.6%), of the number of Euphausia pacifica in the water column during the investigation (Table 1). Occurrence of NI was restricted to the upper 20 m at noon and in the afternoon, and below 30 m during the early morning (03:00–09:00) and at 20–50 m at night (Fig. 4). The abundance of NI at each sampling point was usually low, and the maximum concentration was recorded at 06:00 (1.3 ind. m 3) (Table 2). The WMDs of NI varied from 13.9 to 55.4 m (mean= 32.2 m, Fig. 5). NI showed no DVM. NII also played a relatively insignificant role in the numerical abundance composition of the Euphausia pacifica population,
contributing only 0.2–5.3%, (mean =1.7%), to the total population (Table 1). NII occurred nearly throughout the water column, but mostly aggregated below 30 m (Figs. 2F and 4). Highest abundances of NII were recorded after dawn (1.3 ind. m 3 at 6:00), before dusk (1.4 ind. m 3 at 18:00) or in the early evening (1.5 ind. m 3 at 21:00) (Table 2). The WMDs of NII ranged from 27.5 to 47.8 m (mean= 39.7 m, Fig. 5). No diel vertical migration occurred in this stage. MN was relatively abundant, and made up 1.4–11.2%, (mean= 5.1%), of the Euphausia pacifica population (Table 1). It was distributed throughout the water column (Figs. 2G and 4), and its abundance changed little except at dusk (15:00 both on 2 and 3 May) and around mid night (24:00 and 03:00) when the abundance was relatively low (Table 2). The WMDs of MN varied between 16.4 and 44.4 m, (mean =26.4 m, Fig. 5), and showed no DVM. The vertical distributions of CI–CIII were similar. They were all important components of the Euphausia pacifica population, accounting for 1.3–16.6% (mean= 10.7%), 2.1–22.6% (mean= 12.1%) and 0.6–14.9% (mean = 7.5%), respectively (Table 1). The vertical distribution of calyptopis stages had an important effect on the vertical distribution of the whole Euphausia pacifica population during the investigation (Fig. 2H). The majority of the individual
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M
80 0
125
250 0
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250 0
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250 0
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250 0
125
250 0
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250 0
125
250
0 20 40 60 T
80
Fig. 4. (Continued)
Table 2 Numerical abundance (ind. m 3) of each developmental stage and total population at each sampling time. Sampling time
Egg NI NII MN CI CII CIII FI FII FIII FIV FV FVI J Female Male total
Day
Night (h)
Day (h)
15:00
18:00
21:00
24:00
03:00
06:00
09:00
12:00
15:00
19.05 0.56 0.41 1.61 4.48 2.57 0.88 0.38 0.12 0.06 0.03 0 0 0 0 0 30.13
45.29 0.03 1.40 3.28 0.67 1.14 0.29 0.47 0.35 0.47 0.09 0.06 0 0 0 0 53.54
18.61 0.20 1.46 3.13 2.16 1.20 0.56 0.15 0.03 0.15 0.15 0 0 0 0.03 0.03 27.85
30.01 0.07 0.90 1.06 2.85 2.75 2.59 0.93 0.93 0.70 0.27 0.03 0 0 0 0 43.07
26.10 0.35 0.82 1.87 7.02 14.13 8.51 2.22 0.44 0.50 0.29 0.03 0.03 0 0.03 0.06 62.40
22.47 1.32 1.29 3.45 10.47 14.66 10.44 4.45 1.02 0.38 0.18 0.06 0 0.03 0 0.06 70.27
20.92 0.25 0.40 4.57 8.83 10.13 5.47 1.77 0.50 0.28 0.06 0 0 0 0.03 0 53.22
86.54 0.03 0.40 3.20 12.68 12.71 8.98 5.72 1.71 0.71 0.22 0.03 0.03 0 0 0 132.98
44.73 0 0.15 1.14 11.00 13.19 8.63 3.80 0.53 0.29 0 0 0 0 0 0 83.47
calyptopis were distributed in the upper 10 m from 15:00 on 2 May to 03:00 on 3 May, and at 0–30 m from 06:00 to 15:00 on 3 May (Fig. 4), and their abundances were relatively lower from 15:00 to 24:00 on 2 May than from 03:00 to 15:00 on 3 May (Fig. 4, Table 2). The WMDs of CI ranged from 8.7 to 24.5 m (mean= 14.3 m). The WMDs of CII–CIII focused above 20 m and
ranged from 6.6 to 16.4 m (mean = 11.7 m) and 6.4 to 15.0 m (mean= 10.6 m), respectively (Fig. 5). CI exhibited a weak DVM, while CII and CIII showed moderate DVM. Furcilia stages, especially the young furcilia stages, showed a similar pattern of diel vertical distribution as calyptopis (Figs. 2I and 4). FI was the most abundant furcilia stage, accounting for
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0 10 9.3
20
6.4
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11.6
15.0 14.0 15.0
30 30.9 31.2
40 50
31.0
34.7
36.7
39.1
42.4
44.0
47.2
60 Egg
70
CIII
0 10 20
8.1 13.9
30
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30
5.0 10.8
14.9 14.3 16.4
15.0 20.0
23.3
25.0
40 32
50 60 70
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Fig. 5. The weighted mean depth (WMD) of each developmental stage of Euphausia pacifica at each sampling time. NI–NII: nauplius stage; MN: metanauplius stage; CI–CIII: calyptopis stage; FI–FVI: furcilia stage; J: juvenile; F: female; M: male.
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15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
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0 10
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Fig. 5. (Continued)
0.5–6.3%, (mean =3.0%), of the whole Euphausia pacifica population (Table 1). The WMDs of FI ranged from 6.5 to 21.0 m, (mean= 13.6 m), with the daytime WMDs deeper than nighttime WMDs (Fig. 5). FI showed a somewhat similar trend of DVM as late calyptopis. The contribution of FII to the total population was low, only accounting for 0.1 to 2.2%, (mean = 0.9%, Table 1). The WMDs of FII varied between 8.4 and 24.3 m (mean =17.7 m, Fig. 5). FII showed an obvious DVM. FIII contributed 0.2 to 1.6%, (mean= 0.7%), to the total Euphausia pacifica population (Table 1). The WMDs of this stage varied from 6.4 to 27.7 m (mean = 17.4 m, Fig. 5), and showed a clear DVM behavior. The abundance of FIV–FVI was very low in the water column (Table 2). FIV contributed 0–0.6% (mean = 0.3%), to the total population (Table 1). The WMDs of FIV ranged from 5.0 to 40.0 m (mean =19.9 m), and there was a strong DVM trend in this stage (Fig. 5). Stage FV– FVI were often absent during the investigation, i.e., FV was absent 4 out of 9 times and FVI, 7 out of 9 times (Fig. 4). However it still can be seen that these two stages exhibit a DVM behavior. Juveniles were nearly absent during the investigation, and were only obtained once (Fig. 4). Both female and male adults occurred 3 times during the investigation, and the former seemed to undergo DVM, and the latter showed no evidence of DVM (Figs. 4 and 5). In addition to DVM, Euphausia pacifica exhibited an ontogenetic migration, which was apparent due to the high-frequency sampling. During the investigation period, spawning apparently took place at 20–50 m depth, hatched nauplii sank a little, metanauplius began moving toward the surface, calyptopis larvae reached the uppermost layer, furcilia larvae began DVM and deepened their daytime residence depth as they grew (Figs. 4 and 5). Eggs were commonly distributed below 20 m, concentrated in or near the high chlorophyll a concentration layer, in waters with temperatures lower than 9 1C, and a relatively wide range in salinity. Nauplius stages (NI, NII) existed a little deeper than eggs, concentrated below 30 m, in an area of relatively low temperature, high salinity and low chlorophyll a (Figs. 2 and 4). MN were distributed through the whole water column, spanning a wide range of temperature, salinity and chlorophyll a, but higher concentrations were usually found in the upper 30 m, where temperature and chlorophyll a concentration were relatively high (Figs. 2 and 4). CI–CIII were abundant in the upper 30 m, where temperatures were relatively high (usually higher than 9 1C),
salinity was variable, and near or in the chlorophyll a concentration center. Furcilia individuals were distributed in a very similar pattern to the calyptopis, but during the daytime high furcilia concentrations were usually found deeper than calyptopis. Juveniles, female adults and male adults were collected only at nighttime or at dawn during the investigation (Fig. 4), and they usually were not found near the high chlorophyll a center (Figs. 2 and 4). In conclusion, eggs and nauplius individuals were apt to distribute in a relatively lower temperature. MN showed a weak relationship with temperature and chlorophyll a. Calyptopis and furcilia individuals were associated with relatively high temperature and high chlorophyll a concentrations, while post-larval stages seemed to avoid the high chlorophyll a concentration center. Salinity seemed to have very little influence on the vertical distribution of Euphausia pacifica population.
4. Discussion and conclusion The larval developmental pathways of Euphausia pacifica vary with geographical regions (Boden, 1950; Endo and Komaki, 1979; Ross, 1981; Suh et al., 1993; Feinberg et al., 2006). During our study, we found that the larval development of Euphausia pacifica was the same as that documented by Suh et al. (1993). Thus, we chose to identify the larval stages of Euphausia pacifica primarily according to the classifications proposed by Suh et al. (1993). DVM behavior is a common phenomenon in euphausiids (e.g., Brinton, 1967; Youngbluth, 1976; Sameoto, 1980; Hirota et al., 1984; Barange, 1990; Iguchi, 1995; Taki, 2003). Studies concerned with the diel vertical distribution and DVM of Euphausia pacifica have been carried out by many authors (Brinton, 1967; Cooney, 1971; Frost and McCrone, 1974; Youngbluth, 1976; Terazaki et al., 1986; Bollens et al., 1992; Iguchi, 1995; Yoon et al., 2000; Taki, 2003; Endo and Yamano, 2006). But, most of these studies were concerned with the post-larval stages and/or size classed larval stages (Brinton, 1967; Frost and McCrone, 1974; Youngbluth, 1976; Iguchi et al., 1993; Endo and Yamano, 2006), only a few (e.g., Iguchi, 1995; Taki, 2003) were related to all developmental stages. Our study dealt with the diel vertical distribution and migration of all developmental stages of Euphausia pacifica on the basis of a higher sampling frequency (9 times a day) than usual (2 times a day), and thus can give a clearer pattern of variations in vertical distribution throughout the day as well as migration.
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The pattern of diel vertical distribution and migration of Euphausia pacifica differs with developmental stage. Cooney (1971) found segregation of size classes of Euphausia pacifica within the vertical layer in Puget Sound, Washington, with larger euphausiids residing progressively deeper, and with the largest euphausiids occurring almost exclusively in the bottom-most portion (65–70 m) of the scattering layer. Terazaki et al. (1986) found Euphausia pacifica adults performed DVM, while larvae exhibited very weak or nonexistent DVM in the vicinity of Otsuchi, northeastern Japan. Bollens et al. (1992) reported that adults and juveniles of Euphausia pacifica sampled in Dabob Bay, Washington, always exhibited DVM, while larval Euphausia pacifica showed greater variability in their vertical distributions and exhibited highly variable DVM behavior in different seasons or years. In our study Euphausia pacifica also showed different vertical distribution and migration pattern with different developmental stages. Post-calyptopis stages appeared gradually deeper with increased stage, and the amplitude of DVM also became larger as the development progressed. The diel vertical distribution and abundance of eggs have rarely been reported compared with other developmental stages. Iguchi (1995) studied the vertical distribution and numerical abundance of eggs in Toyama Bay, Southern Japan Sea. His results showed that eggs were distributed throughout the water column, and the abundance of eggs did not change remarkably vertically throughout the day and night, except at 60 m during the day where the egg abundance showed a notable peak. In our study, eggs were distributed nearly throughout the water column (Fig. 4), dominated the Euphausia pacifica population at each sampling time (Table 1), and influenced the vertical distribution pattern of the whole Euphausia pacifica population at most of the sampling times (Fig. 4). Egg abundance was relatively higher during the day than at night in this study, with the highest and the lowest abundances recorded at 12:00 and 21:00, respectively (Table 2). Egg density decreased gradually from 24:00 to 09:00 and increased sharply at 12:00 (Table 2). Our experimental studies carried out at this station during the investigation showed that most gravid females obtained at night (02:30) laid their eggs in the morning (at 09:30 h, Liu and Sun, 2002). Another study from our program that concerned the diel vertical distribution of Euphausia pacifica in spring in the South Yellow Sea showed the highest egg density occurred in the afternoon (15:00, Tao et al., unpubl. MS). Thus, we speculated that eggs were mainly laid around dawn or in the morning. Iguchi (1995) also indicated that eggs were laid before dawn, because the peak abundance was also found during the day and the newly laid eggs were dominant in the day (09:29–12:00) in the upper surface, and constituted only a small part of the sample in the deep water at night (21: 43–00:20) (Iguchi, 1995, Table 2). Many authors studied the diel vertical distribution and DVM of Euphausia pacifica at relatively deep stations, and they indicated that adult Euphausia pacifica always resided in the upper 100 m during the nighttime and sank down to deeper waters during the daytime (Brinton, 1967; Alton and Blackburn, 1972; Frost and McCrone, 1974; Youngbluth, 1976; Iguchi, 1995; Endo and Yamano, 2006). In our study, the maximum sampling depth is 68 m, and results showed that female adults went up into the upper 20 m at night and sank down into deeper waters below 30 m during the day, whereas the adult males did not exhibit normal DVM behavior. Tarling (2003) also found a difference in DVM between male and female Meganyctiphanes norvegica in the Clyde Sea, with females migrating closer to the surface at night than males of equivalent size. Terazaki et al. (1986) sampled at a station of 80 m depth off northeastern Japan, and he found that adult Euphausia pacifica were distributed below 30 m by day and
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stayed at 5–30 m by night. This pattern is very similar to the distribution of female adults in our study. Bollens et al. (1992) studied the vertical distribution and DVM of Euphausia pacifica at a 193 m deep station in Dabob Bay, Washington. He indicated that all size classes of Euphausia pacifica were distributed in the upper 25 m at night irrespective of season or year. In our study there is also a trend that shows from CI onward, the night dwelling WMD were mostly distributed in the upper 20 m. Mauchline and Fisher (1969) mentioned that from calyptopis II onward euphausiid larvae start to show DVM. Iguchi (1995) studied the DVM of each developmental stage of Euphausia pacifica in Toyama Bay, southern Japan Sea. He found that calyptopis stages are not migratory; FII was the first stage to show clear DVM behavior. Taki (2003) reported that the calyptopis stage of Euphausia pacifica underwent DVM in the mid-deeper layer in the coastal areas. In our study, calyptopis stages showed weak or moderate DVM behavior, while from FII on, an obvious DVM was seen. Consistent with the reports of previous authors (e.g., Iguchi, 1995; Endo and Yamano, 2006), we also found the amplitude of the DVM increased with developmental stage. A phenomenon often coincident with the DVM is ontogenetic migration, i.e. with the progression of stages, the dwelling depth decreased or increased. Youngbluth (1976) found the DVM of larval and juvenile Euphausia pacifica varied ontogenetically with the range of migration and proportion of the population migrating increasing with developmental stage. In this paper, the mean WMDs of NI and NII were 32.2 and 39.8 m, respectively, showing a downward ontogenetic migration. Metanauplius went up to 26.4 m. Calyptopis stages showed an upward ontogenetic migration, with the mean WMDs decreasing from CI (14.3 m) to CIII (10.6 m). The furcilia stages again showed a downward ontogenetic migration, with FI residing much shallower (mean DVM=13.6 m), and the later stages much deeper (FIV, 19.9; FVI, 22.5 m) (Fig. 5). In the California Current, daytime vertical distribution of adult Euphausia pacifica was limited to the waters with a temperature of o10 1C (Brinton, 1976). Taki et al. (1996) reported that both juvenile and adult Euphausia pacifica were abundant in the water column when the average temperature was 7–14 1C off Onagawa, Miyagi Prefecture, Japan. Iguchi and Ikeda (1994) suggested that Euphausia pacifica from Toyama Bay, southern Japan Sea is capable of tolerating much wider temperature ranges 5–20 1C. In the present study, the temperature range of 7.5–12.7 1C just fell within the range of the suitable temperature indicated by the above authors. Our data showed that eggs and nauplius were found in a relatively lower temperature range than calyptopis and furcilia, while adults seemed acclimated to the temperature range of the whole water column. As for the chlorophyll a, there is a similar trend as the spatial distribution of Euphausia pacifica (Yoon et al., 2000), i.e. calyptopis and furcilia were distributed near or in the subsurface maximum high chlorophyll a depth, while the adults seemed to avoid it. The salinity, as mentioned by many other authors, was not a restricting factor for the vertical distribution and migration of Euphausia pacifica in this study. Net avoidance by larger individuals, i.e. post-larval stages of euphausiids, and extrusion through the net meshes of small-sized individuals, such as nauplius and metanauplius, have been well discussed in many previous studies (e.g., Mauchline and Fisher, 1969; Brinton, 1967; Yoon et al., 2000). Different authors have data about what mesh size is suitable for a sampling of specific stages. Hirota et al. (1984) indicated that nauplius larvae of E. nana (around 3 mm) were hardly collected by the 0.33 mm mesh size net. However, Endo and Yamano (2006) suggested that the vertical net (0.333 mm mesh size) data had no bias in abundance of 2 mm individuals due to escapement/extrusion. The low abundance of nauplius and the near absence of post-larval stages in our study suggests that the sampling device might not
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be appropriate for collecting all development stages of Euphausia pacifica. The mesh size (0.32 mm) might be too coarse to sample all the individuals of nauplius stages. The pulsed laying of eggs might also cause periods of lower nauplii abundance since these are relatively short-lived stages (Feinberg et al., 2006). Post-larval stages were likely able to avoid the net due to the small mouth diameter (0.8 m). The deepest sampling depth was 68, 2 m above the bottom. This may not be able to cover the whole distribution range of the post-larval stages because these stages may reside just above the bottom during the daytime. Thus, our data may not be conclusive for nauplius and post-larval stages. A survey with larger nets and somewhat smaller mesh size should be used in future investigations to resolve this problem.
Acknowledgments This work was supported by National Natural Science Foundation of PR China no. 40306021, and by the Science and Technology Department of PRChina (program no. 2006CB400606). We thank the crew of the R/V dongfanghong-2 for their assistance in collecting samples. We thank H. Wei for providing CTD data and Prof. R.-H. Li for chlorophyll a data. We thank Prof. Q. Zhang for help with water density calculations. We also thank the two reviewers for helpful comments, Leah Feinberg for correcting the English, and both Leah and and Bill Peterson for their valuable comments and suggestions for ways to improve the manuscript. References Alton, M.S., Blackburn, C.J., 1972. Diel changes in the vertical distributions of the euphausiids, Thysanoessa spinifera Holmes and Euphausia pacifica Hansen in the coastal waters of Washington. California Fish and Game 58, 179–190. Anon, 1977. Study on plankton in China Seas. In: Anon (ed.), Scientific Reports of Comprehensive Oceanography Expedition in China Seas, Ocean Research Office Press, Tianjin vol. 8, pp. 1–159. (in Chinese). Barange, M., 1990. Vertical migration and habitat partitioning of six euphausiid species in the northern Benguela upwelling system. Journal of Plankton Research 12, 1223–1237. Boden, B.P., 1950. The post-naupliar stages of the crustacean Euphausia pacifica. Transactions of the American Microscopical Society 69, 373–386. Bollens, S.M., Frost, B.W., Lin, T.S., 1992. Recruitment, growth, and diel vertical migration of Euphausia pacifica in a temperate fjord. Marine Biology 114, 219–228. Brinton, 1962. The distribtution of Pacific euphausiids. Bulletin of the Scripps Institution of Oceanography 8, 51–269. Brinton, E., 1967. Vertical migration and avoidance capability of euphausiids in the California Current. Limnology and Oceanography 12, 451–483. Brinton, E., 1976. Population biology of Euphausia pacifica off Southern California. Fish. Bull. U.S 74, 733–762. Cai, B., 1982. The preliminary study on the classification of euphausiids in the East China Sea and Southern Yellow Sea. Marine Science Bulletin 1 (4), 68–78 in Chinese. Cai, B., 1986. The distribution of the Euphausiacea in the Huanghai Sea and East China Sea. Transactions of Chinese Crustacean Society 1, 140–146 in chinese. Chen, Q., Chen, Y., Hu, Y., 1980. Preliminary study on the plankton communities in the southern Yellow Sea and the East China Sea. Acta Oceanologica Sinica 2 (2), 149–157 in Chinese. Cooney, R.T., 1971. Zooplankton and micronekton associated with a diffuse soundscattering layer in Puget Sound, Washington. Ph.D. Thesis, University of Washington, Seattle, Washington. Endo, Y., 1984. Daytime surface swarming of Euphausia pacifica (Crustacea: Euphausiacea) in the Sanriku coastal waters off northeastern Japan. Marine Biology 79, 269–276. Endo, Y., 2000a. Distribution and standing stock 3.1 Japanese waters. In: Everson, I. (Ed.), Krill: Bilology, Ecology and Fisheries. Blackwell Science, pp. 40–52. Endo, Y., 2000b. Role of Krill in Marine Food Webs, 7.1 Japanese waters. In: Everson, I. (Ed.), Krill: Biology, Ecology and Fisheries. Blackwell Science, pp. 182–189. Endo, Y., 2000c. Management of Krill Fisheries in Japanese Waters. In: Everson, I. (Ed.), Krill: Biology, Ecology and Fisheries. Blackwell Science, pp. 284–299. Endo, Y., Komaki, Y., 1979. Larval stages of euphausiids with descriptions of those of Thysanoessa longipes. Brandt. Bull. Japan Sea reg. Fish. Res. Lab. 30, 97–110. Endo, Y., Yamano, F., 2006. Diel vertical migration of Euphausia pacifica (Crustacea, Euphausiacea) in relation to molt and reproductive processes, and feeding activity. Journal of Oceanography 62, 693–703.
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Diel vertical distribution and migration of a euphausiid Euphausia pacifica in the Southern Yellow Sea Hui-Lian Liu a, Song Sun b,n a b
Department of Marine Organism Taxonomy and Phylogeny, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
a r t i c l e in f o
a b s t r a c t
Article history: Accepted 30 October 2009 Available online 11 November 2009
Stage-specific differences in the diel vertical distribution and migration of a euphausiid, Euphausia pacifica, were studied at a single station (E2, 70 m water depth) in the South Yellow Sea, by sampling with a conical closing net from five discrete strata, every 3 h, for 24 h, on 2–3 May 2001. Environmental data were collected simultaneously with the net sampling. Results showed that eggs contributed a large proportion of the numerical abundance of the Euphausia pacifica population throughout the investigation. They were mainly distributed below 20 m depth, and concentrated in the 30–50 m strata throughout the day and night. Nauplius stage I (NI) was distributed below 10 m, and seldom occurred in the upper 10 m. Nauplius stage II (NII) and Metanauplius stage (MN) extended their distribution to nearly the whole water column; however, the MN resided somewhat shallower than NII. The majority of calyptopis stages I to III (CI to CIII ) and early furcilia stages I to III (FI to FIII) were restricted to the upper 30 m throughout the day. The weighted mean depth tended to increase as the stage progressed from stage FI onward. Calyptopis stages showed a weak or moderate diel vertical migration behavior, and the onset of an obvious diel vertical migration took place in FII stage. The amplitude of the diel vertical migration varied with developmental stages. Stages after FIV were often absent from samples during the investigation, but from the limited available data, DVM occurred from stages FIV–VI and female adults. However, the male adults showed a somewhat different migration behavior. In summary, an ontogenetic migration pattern is obvious from this high-frequency sampling: spawning took place at 20–50 m depth, hatched nauplii sank a little, metanauplius began moving toward the surface, and calyptopis larvae reached the uppermost layer. Furcilia larvae began DVM and deepened their daytime residence depth with age. The vertical distribution of Euphausia pacifica seemed to relate to temperature and chlorophyll a. & 2009 Elsevier Ltd. All rights reserved.
Topical issue on ‘‘Krill Biology and Ecology.’’ The issue is compiled and guest-edited by the North Pacific Marine Science Organization (PICES), International Council for the Exploration of the Sea (ICES), and Global Ocean Ecosystem Dynamics (GLOBEC) project. Keywords: Euphausia pacifica Euphausiid Vertical distribution Diel vertical migration Yellow Sea
1. Introduction Euphausia pacifica is widely distributed in the North Pacific Ocean (Brinton, 1962; Mauchline and Fisher, 1969) and its adjacent coastal waters (Ponomareva, 1966; Ross et al., 1982; Endo, 1984; Cai, 1986; Sawamoto, 1992; Yoon et al. 2000). Off the China coast, Euphausia pacifica is commonly found in the Yellow Sea and the East China Sea (Anon., 1977; Zhang et al., 1991; Wang et al., 2003), especially in the Yellow Sea north of 341N, where this species is the dominant euphausiid species in most seasons (Huang, 1986). Many studies have been carried out on the distribution, life history and fishery of Euphausia pacifica in the past 50 years over its wide range (Nicol and Endo, 1997, Endo, 2000a, b, c). However, studies on this species in the Yellow Sea
n
Corresponding author. E-mail addresses: [email protected] (H.-L. Liu), [email protected] (S. Sun). 0967-0645/$ - see front matter & 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2009.10.009
and the East China Sea are relatively scarce, being confined to species occurrence and morphology descriptions (Hong, 1969; Cai, 1982), abundance and spatial distribution (Chen et al., 1980; Cai, 1986; Yoon et al., 2000; Wang et al., 2003; Wang and Zuo, 2004; Xu and Li, 2005), larval development (Suh et al., 1993; Liu and Sun, 2002) and gut content analysis and feeding (Kang, 1966, 1986). Diel vertical migration of juvenile and adult Euphausia pacifica is well studied (Brinton, 1967; Cooney, 1971; Frost and McCrone, 1974; Youngbluth, 1976; Terazaki et al., 1986; Bollens et al., 1992; Iguchi et al., 1993; Iguchi, 1995; Yoon et al., 2000; Taki, 2003; Nakagawa et al., 2003; Endo and Yamano, 2006), however most of these studies were focused on the post-larval stages. A few studies concerning the diel vertical migration of different stages or size classes were carried out off Japan (Iguchi, 1995; Taki, 2003) or in the north-east Pacific (Bollens et al., 1992); however, the sampling frequency in these studies was usually low. Up to now, little data were obtained on the diel vertical migration of Euphausia pacifica in the Yellow Sea, let alone studies on the DVM of separate developmental stages.
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The purpose of this paper is to present the results of a study of the stage-specific diel vertical distribution and migration of Euphausia pacifica based on high-frequency sampling at a station in the Yellow Sea in spring with a discussion of how the environmental factors might influence the DVM.
595
(1993), Boden (1950) and Cai (1982). Abundances were calculated from volumes filtered (assuming 100% efficiency) as ind. m 3. For each developmental stage, the weighted mean depth (WMD) was calculated according to the equation: WMD= P P ( nidi)/ ni (Frost and Bollens, 1992), where ni is abundance 3 (ind. m ) at depth di, and di is the midpoint of each depth stratum.
2. Materials and methods 2.2. Observation of environmental factors 2.1. Sampling station, sampling protocol and sample analysis Multidisciplinary investigations were carried out during the cruises aboard the R. V. Dongfanghong No. 2 in the East China Sea and the South Yellow Sea from 30 April to 11 May, 2001. A total of seven stations were sampled: E1 (351000 N, 1211000 E, depth: 35 m), E2 (341300 N, 1231060 E, depth: 70 m), E4 (311000 N, 1221300 E, depth: 20 m), E5 (291000 N, 1221300 E, depth: 48 m), E6 (291000 N, 1251300 E, depth: 79 m), P1 (281100 N, 127147.50 E, depth: 1015 m) and P2 (281350 N, 126122.50 E, depth: 195 m). The En (n = 1, 2y) stations were fixed stations (the ship was at anchor) where a series of in situ measurements or samples were taken. E2 is a station in the area of the South Yellow Sea Cold Water Mass (SYCWM) (Zhang et al.,1996) where Euphausia pacifica often aggregate in spring (Anon., 1977). It was chosen for our diel study since, unlike the other stations, Euphausia pacifica are usually abundant here in spring and all stages of Euphausia pacifica can occur there. Zooplankton samples were collected nine times over a 24 h period using a conical closing net (mouth diameter: 0.8 m, length: 2.8 m, mesh opening: 0.32 mm) from 5 strata (0–10, 10–20, 20–30, 30–50 and 50–68 m) at 3 h intervals from 15:00 on 2 May to 15:00 on 3 May 2001 at station E2 (Fig. 1). Each time the towing operations lasted less than 25 min. The times of local sunrise and sunset were around 05:00 and 18:30, respectively. Zooplankton samples were preserved in a 5% formalin-seawater solution immediately after sampling. Each developmental stage, namely, egg, nauplius I–II (NI–II), metanauplius (MN), calyptopis I–III (CI–III), furcilia I–VI (FI–VI), juvenile, female adults and male adults of Euphausia pacifica was sorted and identified using a dissecting microscope according to the descriptions of Suh et al.
38
37
Shandong
36 Yellow Sea
35 E2
34 Jiangsu
33
32 119
Vertical profiles of water temperature, salinity and density were recorded with a CTD system (Sea-Bird SBE 9) down to the bottom at time intervals coinciding with the net samplings. The vertical profiles of chlorophyll a were determined from seawater samples collected at 3 h intervals coinciding with the net sampling from depths of 0, 10 or 12.5, 25, 38 or 40, 50 m, and near the bottom. Water samples (250 ml) were filtered through glass-fiber filters (Whatman GF/F), and then extracted with 90% acetone for 24 h in darkness. The concentration of chlorophyll a was measured using a Turner Designs (Model II) fluorometer calibrated with pure chlorophyll a (Sigma).
3. Results 3.1. Environmental factors Diel vertical variations in temperature at the sampling station are shown in Fig. 2A. Surface water temperature ranged from 11.7 to 12.7 1C, and bottom temperature varied between 8.8 and 9.4 1C. A thermocline of 3 1C difference (ranged from 9 to 11 1C) formed between 15 and 25 m. Intermediate Cold Water (ICW) existed at this station day and night, with a temperature inversion at the depth of about 25–30 m (Figs. 2A and 3A), which varied between 7.5 and 8.3 1C. Below 40 m, temperature was relatively uniform, ranging between 8.5 and 9.4 1C (Figs. 2A and 3A). Salinity varied between 32.31 and 33.27 in the water column during the investigation. Surface salinity ranged from 32.31 to 32.72. A salinity maximum often appeared in the upper water column at the base of the mixed layer, at depths ranging between 10–25 m (Fig. 3B). A salinity minimum (32.35–32.62) occurred at a similar depth as the corresponding temperature minimum. An indistinct halocline existed between 25–40 m (Figs. 2B and 3B). Bottom salinity ranged between 33.01 and 33.27. Chlorophyll a changed significantly from 0.2 to 5.7 mg m 3 in the water column. The chlorophyll maximum was found at 20–30 m with the highest values (2.5–5.7 mg m 3) recorded at 25 m, just under the thermocline. The concentrations above 10 m and below 35 m were usually less than 1.00 mg m 3 (Fig. 2C). Water density increased consistently from the surface to the bottom except at 24:00 h, when surface values were higher and the value at 15 m was obviously lower than the former and the latter sampling times (Fig. 2D). The vertical fine structure of temperature and salinity (Fig. 3) indicated that the upper mixed zone was not well mixed, and this suggested weak intrusions of water masses with different characteristics existed. Especially at 24:00 h, when a water mass with relatively high temperature, high salinity, low chlorophyll a and high water density (kg m 3-1000), came through the surface at the study site (Fig. 2). 3.2. Diel vertical distribution and migration
120
121
122
123
124
125
Fig. 1. Sampling station E2 with superimposed depth contours (20, 50 and 80 m).
Eggs were more abundant than the other components (NI, NII, MN, CI, CII, CIII, FI, FII, FIII, FIV, FV, FVI, juvenile, female adults and
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Sampling time
Sampling time 15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00 0
10
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Depth (m)
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30 40
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sampling time
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
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0
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Depth (m)
Depth (m)
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
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60 70
70
sampling time
sampling time
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00 0
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15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00 0
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60
60
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70
sampling time
sampling time
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
0
0
10
10
20
20
30 40
depth (m)
depth (m)
30
30 40
50
50
60
60
70
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Fig. 2. Diel variations in vertical profiles of temperature (1C), salinity (psu), chlorophll a (mg m 3), water density (kg m 3-1000) and Euphausia pacifica density (ind. m 3) at sampling station from 15:00, 2 May to 15:00, 3 May 2001. A. temperature, B. salinity, C. Chlorophll a, D. water density, E. eggs, F. nauplius, G. metanauplius, H. total calyptopis, I. total furcilia, J. post-larvae, K. total larvae and L. total population.
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(J)
sampling time
sampling time 15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
0
0
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20 depth (m)
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70 sampling time
sampling time
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
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0
0
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20 depth (m)
depth (m)
597
30 40
30 40
50
50
60
60
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Fig. 2. (Continued)
15:00
18:00
21:00
24:00
03:00
06:00
09:00
12:00
15:00
Temperature (°C) 6
10
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6
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14 6
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20 40 60 80 Salinity (psu) 32.0 0
33.0
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33.0
32.0
33.0
32.0
33.0
32.0
33.0
32.0
33.0
32.0
Depth (m)
20 40 60 80 Fig. 3. Vertical profiles of temperature (1C) and salinity (psu) at sampling station at 3 h intervals from 15:00 on 2 May to 15:00 on 3 May, 2001.
33.0
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Table 1 Contribution by % of numerical abundance of each developmental stage to the total abundance of whole Euphausia pacificaa population at each sampling time. Sampling time
Egg NI NII MN CI CII CIII FI FII FIII FIV FV FVI J Female Male
Day
Night
Day
average
15:00
18:00
21:00
24:00
03:00
06:00
09:00
12:00
15:00
63.20 1.84 1.36 5.34 14.85 8.54 2.91 1.26 0.39 0.19 0.10 0 0 0 0 0
84.59 0.05 2.62 6.12 1.26 2.13 0.55 0.87 0.66 0.87 0.16 0.11 0 0 0 0
66.81 0.74 5.25 11.24 7.77 4.31 2.00 0.53 0.11 0.53 0.53 0 0 0 0.11 0.11
69.67 0.15 2.08 2.46 6.62 6.39 6.00 2.16 2.16 1.62 0.62 0.08 0 0 0 0
41.82 0.56 1.31 3.00 11.25 22.64 13.64 3.56 0.70 0.80 0.47 0.05 0.05 0 0.05 0.09
31.97 1.87 1.83 4.91 14.90 20.86 14.86 6.33 1.46 0.54 0.25 0.08 0 0.04 0 0.08
39.31 0.47 0.76 8.59 16.59 19.04 10.28 3.33 0.93 0.53 0.12 0 0 0 0.06 0
65.08 0.02 0.30 2.41 9.54 9.56 6.76 4.30 1.29 0.54 0.16 0.02 0.02 0 0 0
53.59 0 0.18 1.37 13.18 15.81 10.34 4.56 0.63 0.35 0 0 0 0 0 0
57.34 0.64 1.74 5.05 10.66 12.14 7.48 2.99 0.92 0.66 0.27 0.04 0.01 0 0.02 0.03
-3
Abundance (ind. m ) 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200 0
100 200
Depth (m)
0 20 40 60 Egg
80 0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
0 20 40 60
NI
80 0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
0
2
4
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2
4
0
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4
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2
4
0 20 40 60
NII
80 0
5
10 0
5
10 0
5
10 0
5
10 0
5
10 0
5
10 0
5
10 0
5
10 0
5
10
0 20 40 60
MN
80 0
20 40
0
20
40
0
20
40
0
20 40
0
20 40
0
20
40
0
20 40
0
20 40
0
20 40
0 20 40 CI
60 80 0
50
100 0
50
100 0
50
100 0
50
100 0
50
100 0
50
100 0
50
100 0
50
100 0
50
100
0 20 40 60
CII
80
Fig. 4. Vertical distribution in numerical abundance (ind. m 3) of each developmental stage of Euphausia pacifica at 3 h intervals from 15:00, 2 May to 15:00, 3 May 2001. NI–NII: nauplius stage; MN: metanauplius stage; CI–CIII: calyptopis stage; FI–FVI: furcilia stage; J: juvenile; F: female; M: male; T: total population.
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0
30
60 0
30
60 0
30
60 0
30
60 0
30
60 0
30
60 0
599
30
60 0
30
60 0
30
60
0 20 40 CIII 60 80 0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0
10
20
0 20 40 FI
60 80 0
4
8 0
4
8 0
4
8
0
4
8 0
4
8
0
4
8 0
4
8 0
4
8 0
4
8
0 20 40 FII
60 80 0
2
4 0
2
4 0
2
4 0
2
4 0
2
4 0
2
4 0
2
4 0
2
4 0
2
4
0 20 40 60
FIII
80 0
1
2 0
1
2 0
1
2 0
1
2 0
1
2 0
1
2 0
1
2 0
1
2 0
1
2
0 20 40 FIV
60 80 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3
0 20 40 FV
60 80
Fig. 4. (Continued)
male adults), accounting for 32.0–84.6%, (mean=57.3%), of the total number of Euphausia pacifica in the water column during the investigation (Table 1). Eggs were distributed almost throughout the water column, but most commonly occurred below 20 m depth, and aggregated at 30–50 m (Fig. 4). Eggs were more abundant in the daytime than during nighttime, with the maximum abundance appearing at 12:00 (86.5 ind. m 3), and the lowest at 21:00 (18.6 ind. m 3) (Table 2). The WMDs of eggs ranged from 31.0 to 47.2 m, (mean=37.5 m), during the investigation (Fig. 5). The vertical distribution of eggs dominated the vertical distribution pattern of the whole Euphausia pacifica population at most sampling times during the investigation (Figs. 2E and 4). NI contributed only a small portion, 0–1.9%, (mean= 0.6%), of the number of Euphausia pacifica in the water column during the investigation (Table 1). Occurrence of NI was restricted to the upper 20 m at noon and in the afternoon, and below 30 m during the early morning (03:00–09:00) and at 20–50 m at night (Fig. 4). The abundance of NI at each sampling point was usually low, and the maximum concentration was recorded at 06:00 (1.3 ind. m 3) (Table 2). The WMDs of NI varied from 13.9 to 55.4 m (mean= 32.2 m, Fig. 5). NI showed no DVM. NII also played a relatively insignificant role in the numerical abundance composition of the Euphausia pacifica population,
contributing only 0.2–5.3%, (mean =1.7%), to the total population (Table 1). NII occurred nearly throughout the water column, but mostly aggregated below 30 m (Figs. 2F and 4). Highest abundances of NII were recorded after dawn (1.3 ind. m 3 at 6:00), before dusk (1.4 ind. m 3 at 18:00) or in the early evening (1.5 ind. m 3 at 21:00) (Table 2). The WMDs of NII ranged from 27.5 to 47.8 m (mean= 39.7 m, Fig. 5). No diel vertical migration occurred in this stage. MN was relatively abundant, and made up 1.4–11.2%, (mean= 5.1%), of the Euphausia pacifica population (Table 1). It was distributed throughout the water column (Figs. 2G and 4), and its abundance changed little except at dusk (15:00 both on 2 and 3 May) and around mid night (24:00 and 03:00) when the abundance was relatively low (Table 2). The WMDs of MN varied between 16.4 and 44.4 m, (mean =26.4 m, Fig. 5), and showed no DVM. The vertical distributions of CI–CIII were similar. They were all important components of the Euphausia pacifica population, accounting for 1.3–16.6% (mean= 10.7%), 2.1–22.6% (mean= 12.1%) and 0.6–14.9% (mean = 7.5%), respectively (Table 1). The vertical distribution of calyptopis stages had an important effect on the vertical distribution of the whole Euphausia pacifica population during the investigation (Fig. 2H). The majority of the individual
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0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3
0 20 40 FVI
60 80 0
0.15
0.3 0
0.15 0.3 0
0.15
0.3 0
0.15 0.3 0
0.15
0.3
0
0.15 0.3 0
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0.3 0
0.15 0.3 0
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0.3
0 20 40 60
J
80 0
0.15
0.3 0
0.15 0.3 0
0.15
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0.15
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0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3
0 20 40 60
F
80 0
0.15 0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3 0
0.15
0.3
0 20 40 60
M
80 0
125
250 0
125
250 0
125
250 0
125
250 0
125
250 0
125
250 0
125
250 0
125
250 0
125
250
0 20 40 60 T
80
Fig. 4. (Continued)
Table 2 Numerical abundance (ind. m 3) of each developmental stage and total population at each sampling time. Sampling time
Egg NI NII MN CI CII CIII FI FII FIII FIV FV FVI J Female Male total
Day
Night (h)
Day (h)
15:00
18:00
21:00
24:00
03:00
06:00
09:00
12:00
15:00
19.05 0.56 0.41 1.61 4.48 2.57 0.88 0.38 0.12 0.06 0.03 0 0 0 0 0 30.13
45.29 0.03 1.40 3.28 0.67 1.14 0.29 0.47 0.35 0.47 0.09 0.06 0 0 0 0 53.54
18.61 0.20 1.46 3.13 2.16 1.20 0.56 0.15 0.03 0.15 0.15 0 0 0 0.03 0.03 27.85
30.01 0.07 0.90 1.06 2.85 2.75 2.59 0.93 0.93 0.70 0.27 0.03 0 0 0 0 43.07
26.10 0.35 0.82 1.87 7.02 14.13 8.51 2.22 0.44 0.50 0.29 0.03 0.03 0 0.03 0.06 62.40
22.47 1.32 1.29 3.45 10.47 14.66 10.44 4.45 1.02 0.38 0.18 0.06 0 0.03 0 0.06 70.27
20.92 0.25 0.40 4.57 8.83 10.13 5.47 1.77 0.50 0.28 0.06 0 0 0 0.03 0 53.22
86.54 0.03 0.40 3.20 12.68 12.71 8.98 5.72 1.71 0.71 0.22 0.03 0.03 0 0 0 132.98
44.73 0 0.15 1.14 11.00 13.19 8.63 3.80 0.53 0.29 0 0 0 0 0 0 83.47
calyptopis were distributed in the upper 10 m from 15:00 on 2 May to 03:00 on 3 May, and at 0–30 m from 06:00 to 15:00 on 3 May (Fig. 4), and their abundances were relatively lower from 15:00 to 24:00 on 2 May than from 03:00 to 15:00 on 3 May (Fig. 4, Table 2). The WMDs of CI ranged from 8.7 to 24.5 m (mean= 14.3 m). The WMDs of CII–CIII focused above 20 m and
ranged from 6.6 to 16.4 m (mean = 11.7 m) and 6.4 to 15.0 m (mean= 10.6 m), respectively (Fig. 5). CI exhibited a weak DVM, while CII and CIII showed moderate DVM. Furcilia stages, especially the young furcilia stages, showed a similar pattern of diel vertical distribution as calyptopis (Figs. 2I and 4). FI was the most abundant furcilia stage, accounting for
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0 10 9.3
20
6.4
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11.6
15.0 14.0 15.0
30 30.9 31.2
40 50
31.0
34.7
36.7
39.1
42.4
44.0
47.2
60 Egg
70
CIII
0 10 20
8.1 13.9
30
15.0
9.0
6.5
9.6
13.9 14.1
19.7
20.5 21.0
25.0 31.0 30.0
40
37.7
50
49.8
60
55.4
NI
70
FI
0 10 15.8 15.0
30 35.8
40.3 38.4 42.1
44.2
47.8
60
21.2 21.6 21.7
24.3
27.5
40 50
8.4
8.4
20
40.0
41.8
NII
70
22.4
FII
0 10
6.4
20 16.4 30
22.3 28.0 27.1
26.8
40
15.0
17.4 32.2
50
21.1
23.1
7.3
17.8
21.1
18.6
21.8 27.7
44.4
60 MN
70
FIII
0 10 20
9.6
8.7 13.2
30
21.8
10.3 11.8
6.3 14.1 14.2
5.0 13.6
15.0
24.5
25.0
40
21.5
32.4 40.0
50 60
FIV
CI
70 0 10 20
9.4
9.4
6.6
9.2 14.0
30
5.0 10.8
14.9 14.3 16.4
15.0 20.0
23.3
25.0
40 32
50 60 70
CII
FV
Fig. 5. The weighted mean depth (WMD) of each developmental stage of Euphausia pacifica at each sampling time. NI–NII: nauplius stage; MN: metanauplius stage; CI–CIII: calyptopis stage; FI–FVI: furcilia stage; J: juvenile; F: female; M: male.
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15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
15:00 18:00 21:00 24:00 03:00 06:00 09:00 12:00 15:00
0 10
5.0
20
15.0
30 40 40.0
50
40.0
60 70
FVI
F
59.0
0 10
5.0
20
15.0
16.7
30 40 50 50.0
60 70
J
M
Fig. 5. (Continued)
0.5–6.3%, (mean =3.0%), of the whole Euphausia pacifica population (Table 1). The WMDs of FI ranged from 6.5 to 21.0 m, (mean= 13.6 m), with the daytime WMDs deeper than nighttime WMDs (Fig. 5). FI showed a somewhat similar trend of DVM as late calyptopis. The contribution of FII to the total population was low, only accounting for 0.1 to 2.2%, (mean = 0.9%, Table 1). The WMDs of FII varied between 8.4 and 24.3 m (mean =17.7 m, Fig. 5). FII showed an obvious DVM. FIII contributed 0.2 to 1.6%, (mean= 0.7%), to the total Euphausia pacifica population (Table 1). The WMDs of this stage varied from 6.4 to 27.7 m (mean = 17.4 m, Fig. 5), and showed a clear DVM behavior. The abundance of FIV–FVI was very low in the water column (Table 2). FIV contributed 0–0.6% (mean = 0.3%), to the total population (Table 1). The WMDs of FIV ranged from 5.0 to 40.0 m (mean =19.9 m), and there was a strong DVM trend in this stage (Fig. 5). Stage FV– FVI were often absent during the investigation, i.e., FV was absent 4 out of 9 times and FVI, 7 out of 9 times (Fig. 4). However it still can be seen that these two stages exhibit a DVM behavior. Juveniles were nearly absent during the investigation, and were only obtained once (Fig. 4). Both female and male adults occurred 3 times during the investigation, and the former seemed to undergo DVM, and the latter showed no evidence of DVM (Figs. 4 and 5). In addition to DVM, Euphausia pacifica exhibited an ontogenetic migration, which was apparent due to the high-frequency sampling. During the investigation period, spawning apparently took place at 20–50 m depth, hatched nauplii sank a little, metanauplius began moving toward the surface, calyptopis larvae reached the uppermost layer, furcilia larvae began DVM and deepened their daytime residence depth as they grew (Figs. 4 and 5). Eggs were commonly distributed below 20 m, concentrated in or near the high chlorophyll a concentration layer, in waters with temperatures lower than 9 1C, and a relatively wide range in salinity. Nauplius stages (NI, NII) existed a little deeper than eggs, concentrated below 30 m, in an area of relatively low temperature, high salinity and low chlorophyll a (Figs. 2 and 4). MN were distributed through the whole water column, spanning a wide range of temperature, salinity and chlorophyll a, but higher concentrations were usually found in the upper 30 m, where temperature and chlorophyll a concentration were relatively high (Figs. 2 and 4). CI–CIII were abundant in the upper 30 m, where temperatures were relatively high (usually higher than 9 1C),
salinity was variable, and near or in the chlorophyll a concentration center. Furcilia individuals were distributed in a very similar pattern to the calyptopis, but during the daytime high furcilia concentrations were usually found deeper than calyptopis. Juveniles, female adults and male adults were collected only at nighttime or at dawn during the investigation (Fig. 4), and they usually were not found near the high chlorophyll a center (Figs. 2 and 4). In conclusion, eggs and nauplius individuals were apt to distribute in a relatively lower temperature. MN showed a weak relationship with temperature and chlorophyll a. Calyptopis and furcilia individuals were associated with relatively high temperature and high chlorophyll a concentrations, while post-larval stages seemed to avoid the high chlorophyll a concentration center. Salinity seemed to have very little influence on the vertical distribution of Euphausia pacifica population.
4. Discussion and conclusion The larval developmental pathways of Euphausia pacifica vary with geographical regions (Boden, 1950; Endo and Komaki, 1979; Ross, 1981; Suh et al., 1993; Feinberg et al., 2006). During our study, we found that the larval development of Euphausia pacifica was the same as that documented by Suh et al. (1993). Thus, we chose to identify the larval stages of Euphausia pacifica primarily according to the classifications proposed by Suh et al. (1993). DVM behavior is a common phenomenon in euphausiids (e.g., Brinton, 1967; Youngbluth, 1976; Sameoto, 1980; Hirota et al., 1984; Barange, 1990; Iguchi, 1995; Taki, 2003). Studies concerned with the diel vertical distribution and DVM of Euphausia pacifica have been carried out by many authors (Brinton, 1967; Cooney, 1971; Frost and McCrone, 1974; Youngbluth, 1976; Terazaki et al., 1986; Bollens et al., 1992; Iguchi, 1995; Yoon et al., 2000; Taki, 2003; Endo and Yamano, 2006). But, most of these studies were concerned with the post-larval stages and/or size classed larval stages (Brinton, 1967; Frost and McCrone, 1974; Youngbluth, 1976; Iguchi et al., 1993; Endo and Yamano, 2006), only a few (e.g., Iguchi, 1995; Taki, 2003) were related to all developmental stages. Our study dealt with the diel vertical distribution and migration of all developmental stages of Euphausia pacifica on the basis of a higher sampling frequency (9 times a day) than usual (2 times a day), and thus can give a clearer pattern of variations in vertical distribution throughout the day as well as migration.
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The pattern of diel vertical distribution and migration of Euphausia pacifica differs with developmental stage. Cooney (1971) found segregation of size classes of Euphausia pacifica within the vertical layer in Puget Sound, Washington, with larger euphausiids residing progressively deeper, and with the largest euphausiids occurring almost exclusively in the bottom-most portion (65–70 m) of the scattering layer. Terazaki et al. (1986) found Euphausia pacifica adults performed DVM, while larvae exhibited very weak or nonexistent DVM in the vicinity of Otsuchi, northeastern Japan. Bollens et al. (1992) reported that adults and juveniles of Euphausia pacifica sampled in Dabob Bay, Washington, always exhibited DVM, while larval Euphausia pacifica showed greater variability in their vertical distributions and exhibited highly variable DVM behavior in different seasons or years. In our study Euphausia pacifica also showed different vertical distribution and migration pattern with different developmental stages. Post-calyptopis stages appeared gradually deeper with increased stage, and the amplitude of DVM also became larger as the development progressed. The diel vertical distribution and abundance of eggs have rarely been reported compared with other developmental stages. Iguchi (1995) studied the vertical distribution and numerical abundance of eggs in Toyama Bay, Southern Japan Sea. His results showed that eggs were distributed throughout the water column, and the abundance of eggs did not change remarkably vertically throughout the day and night, except at 60 m during the day where the egg abundance showed a notable peak. In our study, eggs were distributed nearly throughout the water column (Fig. 4), dominated the Euphausia pacifica population at each sampling time (Table 1), and influenced the vertical distribution pattern of the whole Euphausia pacifica population at most of the sampling times (Fig. 4). Egg abundance was relatively higher during the day than at night in this study, with the highest and the lowest abundances recorded at 12:00 and 21:00, respectively (Table 2). Egg density decreased gradually from 24:00 to 09:00 and increased sharply at 12:00 (Table 2). Our experimental studies carried out at this station during the investigation showed that most gravid females obtained at night (02:30) laid their eggs in the morning (at 09:30 h, Liu and Sun, 2002). Another study from our program that concerned the diel vertical distribution of Euphausia pacifica in spring in the South Yellow Sea showed the highest egg density occurred in the afternoon (15:00, Tao et al., unpubl. MS). Thus, we speculated that eggs were mainly laid around dawn or in the morning. Iguchi (1995) also indicated that eggs were laid before dawn, because the peak abundance was also found during the day and the newly laid eggs were dominant in the day (09:29–12:00) in the upper surface, and constituted only a small part of the sample in the deep water at night (21: 43–00:20) (Iguchi, 1995, Table 2). Many authors studied the diel vertical distribution and DVM of Euphausia pacifica at relatively deep stations, and they indicated that adult Euphausia pacifica always resided in the upper 100 m during the nighttime and sank down to deeper waters during the daytime (Brinton, 1967; Alton and Blackburn, 1972; Frost and McCrone, 1974; Youngbluth, 1976; Iguchi, 1995; Endo and Yamano, 2006). In our study, the maximum sampling depth is 68 m, and results showed that female adults went up into the upper 20 m at night and sank down into deeper waters below 30 m during the day, whereas the adult males did not exhibit normal DVM behavior. Tarling (2003) also found a difference in DVM between male and female Meganyctiphanes norvegica in the Clyde Sea, with females migrating closer to the surface at night than males of equivalent size. Terazaki et al. (1986) sampled at a station of 80 m depth off northeastern Japan, and he found that adult Euphausia pacifica were distributed below 30 m by day and
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stayed at 5–30 m by night. This pattern is very similar to the distribution of female adults in our study. Bollens et al. (1992) studied the vertical distribution and DVM of Euphausia pacifica at a 193 m deep station in Dabob Bay, Washington. He indicated that all size classes of Euphausia pacifica were distributed in the upper 25 m at night irrespective of season or year. In our study there is also a trend that shows from CI onward, the night dwelling WMD were mostly distributed in the upper 20 m. Mauchline and Fisher (1969) mentioned that from calyptopis II onward euphausiid larvae start to show DVM. Iguchi (1995) studied the DVM of each developmental stage of Euphausia pacifica in Toyama Bay, southern Japan Sea. He found that calyptopis stages are not migratory; FII was the first stage to show clear DVM behavior. Taki (2003) reported that the calyptopis stage of Euphausia pacifica underwent DVM in the mid-deeper layer in the coastal areas. In our study, calyptopis stages showed weak or moderate DVM behavior, while from FII on, an obvious DVM was seen. Consistent with the reports of previous authors (e.g., Iguchi, 1995; Endo and Yamano, 2006), we also found the amplitude of the DVM increased with developmental stage. A phenomenon often coincident with the DVM is ontogenetic migration, i.e. with the progression of stages, the dwelling depth decreased or increased. Youngbluth (1976) found the DVM of larval and juvenile Euphausia pacifica varied ontogenetically with the range of migration and proportion of the population migrating increasing with developmental stage. In this paper, the mean WMDs of NI and NII were 32.2 and 39.8 m, respectively, showing a downward ontogenetic migration. Metanauplius went up to 26.4 m. Calyptopis stages showed an upward ontogenetic migration, with the mean WMDs decreasing from CI (14.3 m) to CIII (10.6 m). The furcilia stages again showed a downward ontogenetic migration, with FI residing much shallower (mean DVM=13.6 m), and the later stages much deeper (FIV, 19.9; FVI, 22.5 m) (Fig. 5). In the California Current, daytime vertical distribution of adult Euphausia pacifica was limited to the waters with a temperature of o10 1C (Brinton, 1976). Taki et al. (1996) reported that both juvenile and adult Euphausia pacifica were abundant in the water column when the average temperature was 7–14 1C off Onagawa, Miyagi Prefecture, Japan. Iguchi and Ikeda (1994) suggested that Euphausia pacifica from Toyama Bay, southern Japan Sea is capable of tolerating much wider temperature ranges 5–20 1C. In the present study, the temperature range of 7.5–12.7 1C just fell within the range of the suitable temperature indicated by the above authors. Our data showed that eggs and nauplius were found in a relatively lower temperature range than calyptopis and furcilia, while adults seemed acclimated to the temperature range of the whole water column. As for the chlorophyll a, there is a similar trend as the spatial distribution of Euphausia pacifica (Yoon et al., 2000), i.e. calyptopis and furcilia were distributed near or in the subsurface maximum high chlorophyll a depth, while the adults seemed to avoid it. The salinity, as mentioned by many other authors, was not a restricting factor for the vertical distribution and migration of Euphausia pacifica in this study. Net avoidance by larger individuals, i.e. post-larval stages of euphausiids, and extrusion through the net meshes of small-sized individuals, such as nauplius and metanauplius, have been well discussed in many previous studies (e.g., Mauchline and Fisher, 1969; Brinton, 1967; Yoon et al., 2000). Different authors have data about what mesh size is suitable for a sampling of specific stages. Hirota et al. (1984) indicated that nauplius larvae of E. nana (around 3 mm) were hardly collected by the 0.33 mm mesh size net. However, Endo and Yamano (2006) suggested that the vertical net (0.333 mm mesh size) data had no bias in abundance of 2 mm individuals due to escapement/extrusion. The low abundance of nauplius and the near absence of post-larval stages in our study suggests that the sampling device might not
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be appropriate for collecting all development stages of Euphausia pacifica. The mesh size (0.32 mm) might be too coarse to sample all the individuals of nauplius stages. The pulsed laying of eggs might also cause periods of lower nauplii abundance since these are relatively short-lived stages (Feinberg et al., 2006). Post-larval stages were likely able to avoid the net due to the small mouth diameter (0.8 m). The deepest sampling depth was 68, 2 m above the bottom. This may not be able to cover the whole distribution range of the post-larval stages because these stages may reside just above the bottom during the daytime. Thus, our data may not be conclusive for nauplius and post-larval stages. A survey with larger nets and somewhat smaller mesh size should be used in future investigations to resolve this problem.
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