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Winter distribution of euphausiids (Euphausiacea) in the Barents Sea (2000–2005)
ARTICLE IN PRESS Deep-Sea Research II 56 (2009) 1959–1967
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Winter distribution of euphausiids (Euphausiacea) in the Barents Sea (2000–2005) Natalia G. Zhukova, Valentina N. Nesterova, Irina P. Prokopchuk , Galina B. Rudneva Polar Research Institute of Marine Fisheries and Oceanography (PINRO), 183038, 6 Knipovich Street, Murmansk, Russia
a r t i c l e in fo
abstract
Article history: Accepted 14 November 2008 Available online 3 December 2008
The purpose of the study is to analyze the state of the Barents Sea euphausiids populations in the warm period (2000–2005) based on the study of their structure dynamics and distribution under the influence of abiotic and biotic factors. For estimation of their aggregations in the bottom layer, the traditional method was used with the help of the modified egg net (0.2 m2 opening area, 564 mm mesh size). The net is used for collecting euphausiids in the autumn–winter period when their activity is reduced, which results in high-catch efficiency. The findings confirmed the major formation patterns of the euphausiids species composition associated with climate change in the Arctic basin. As before, in the warm years, one can see a clear-cut differentiation of space distribution of the dominant euphausiids Thysanoessa genus with localization of the more thermophilic Thysanoessa inermis in the north-west Barents Sea and Thysanoessa raschii in the east. The major euphausiids aggregations are formed of these species. In 2004, the first data of euphausiids distribution in the northern Barents Sea (77–791N) were obtained, and demonstrated extremely high concentrations of T. inermis in this area, with the biomass as high as 1.7–2.4 g m2 in terms of dry weight. These data have improved our knowledge of the distribution and euphausiids abundance during periods of elevated sea-water temperatures in the Barents Sea. The oceanic Atlantic species were found to increase in abundance due to elevated advection to the Barents Sea during the study period. Thus, after nearly a 30-year-long absence of the moderate subtropical Nematoscelis megalops in the Barents Sea, they were found again in 2003–2005. However in comparison with 1960, the north-east border of its distribution considerably shifted to 731500 N 501220 E. The portion of Meganyctiphanes norvegica also varied considerably—from 10% to 20% of the total euphausiids population in the warm 1950s–1960s almost to complete disappearing in 1970–1990s. The peak of this species’ occurrence (18–26%) took place in the beginning of warm period (1999–2000) after a succession of cold years. The subsequent reduction of the relative abundance of M. norvegica to 7% might have been mostly caused by fish predation during a period of low population densities of capelin. This high predation pressure may therefore have been mediated both by other pelagic fishes (i.e. herring, blue whiting, polar cod) but also by demersal fishes such as cod and haddock. Similar sharp fluctuations in the capelin stock (the major consumer of euphausiids) created marked perturbations in the food web in the Barents Sea in the middle 1980s and the early 1990s. & 2008 Elsevier Ltd. All rights reserved.
Keywords: Euphausiids Abundance Distribution Species composition Barents Sea
1. Introduction The fauna of euphausiids in the Barents Sea consists of six species. Thysanoessa inermis, Thysanoessa raschii and Meganyctiphanes norvegica are neritic species, whereas Thysanoessa longicaudata, Nematoscelis megalops and Stylocharion maximum are oceanic (Einarsson, 1945; Drobysheva, 1957, 1994; Lomakina, 1978; Brinton et al., 1999). The three species of Thysanoessa genus are zoogeographical characterized as arcto-boreal organisms, while M. norvegica is a boreal-arctic North-Atlantic species, N. megalops a moderate subtropical species, and S. maximum a
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E-mail address: [email protected] (I.P. Prokopchuk). 0967-0645/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2008.11.007
moderate cold-water tropic species. T. inermis is distributed all over the Barents Sea, predominating in the western areas. T. raschii inhabits mainly the south-eastern shallows, while T. longicaudata is mostly associated with Atlantic waters. The distribution of M. norvegica is also limited by the Atlantic waters (Drobysheva, 1979, 1994; Dalpadado and Skjoldal, 1991, 1996). N. megalops and S. maximum are only rarely advected into the Barents Sea. Some authors (Zelikman, 1958; Drobysheva, 1994; Dalpadado and Skjoldal, 1991, 1996; Timofeev, 2006) estimate euphausiids biomass based on the length-to-weight relation. Euphausiids biomass is highly variable, and reflects local and inter-annual variations in growth conditions, birth, mortality and advection. It is difficult to assess the biomass variability and in particular to understand the underlying causes for these changes. Nevertheless, data are now available that enable us to provide a proxy of the
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entire euphausiids biomass for the Barents Sea, and demonstrate the regional difference for a particular time window. Russian survey data for euphausiids are now available for the years from 2001 to 2005, which is considered as a warm period in the Barents Sea. The objective of this study is to analyze the status of euphausiids population, to estimate their biomass, and thereby improve our understanding of the ecological role of euphausiids in the Barents Sea.
2. Material and methods Regular investigations of euphausiids in the Barents Sea have been carried out by PINRO since 1952. Macro-plankton, i.e. annual monitoring of abundance and distribution of euphausiids during
82° N 80°
78°
I
76° 74° II
72° 70° 68°
0°
10°
20°
30°
40°
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70° E
Fig. 1. Location of plankton sampling stations in the Barents Sea in October– December 2000–2005: (I) The north-eastern Barents Sea and (II) the southern Barents Sea.
autumn–winter (October–December), were included in trawlacoustic surveys of demersal fishes in the Barents Sea. To collect macro-plankton a net (0.2-m2 opening area, 564-mm mesh size) was attached to the headline of a bottom trawl. Macro-plankton was thus sampled at 4–5 m above the bottom (the vertical opening of the bottom trawl). The autumn–winter period is the most effective for euphausiids sampling, as most of the species have reduced vertical migration and are found in more confined habitats at depths than what is true for the spring and summer period. Indices of euphausiids abundance (a number of individuals m3) were calculated by the net attached to trawl catches. In total, 1695 samples were processed in October–December 2000–2005 (Fig. 1, Table 1). A wide area from north of the Spitsbergen archipelago (801N, 101E) to the islands of the Novaya Zemlya and Kolguev (701N, 501E) was covered in the course of the surveys. In 2004, compared with the other years, the northern part of the Barents Sea was studied more thoroughly (791N, 30–401E). These investigated areas are the feeding grounds of both pelagic and demersal fish species. Species composition of euphausiids aggregations with a density of 41000 ind. m3 was studied in the north-western Barents Sea. This area is a core habitat for euphausiids where several species complete their entire life cycle (Drobysheva, 1979). The total length of euphausiid bodies was measured of the rostrum to the end of the telson (Einarsson, 1945). Separation of age groups (years 2002 and 2003 only) was based of length-age keys (Drobysheva, 1994). Biomass calculations were based on length (L) to weight (W) relationships for each of the three main euphausiid species (T. inermis, T. longicaudata, T. raschii) in the Barents Sea according to Eqs. (1)–(3) in Drobysheva and Timofeev (1990). For biomass of M. norvegica new length-to-weight relationships were used the following equation: W ¼ 0:0020L3:3640
for T: inermis
(1)
W ¼ 0:0048L3:0942
for T: longicaudata
(2)
Table 1 Abundance (ind. m3) of euphausiids in the Barents Sea. Year
Ship
Period
Number of stations
Southern Barents Sea
North-western Barents Sea
2000
AtlantNIRO Fridtjof Nansen
October 13–December 7 October 21–December 30
267
548
811
2001
AtlantNIRO Fridtjof Nansen
October 8–December 14 October 26–December 21
285
740
451
2002
Fridtjof Nansen Persey-3 Persey-3
October 16–December 29 November 16–December 8 January 29–March 03
249
1159
1354
2003
Smolensk Fridtjof Nansen G.O. Sars Smolensk
October 16–December 30 November 14–December 25 February 07–March 1 February 2–March 14
373
689
689
2004
Fridtjof Nansen Smolensk G.O. Sars Smolensk
October 13–December 28 October 14–December 29 February 7–March 7 February 9–March 3
318
464
501
2005
Fridtjof Nansen
October 23–December 15
203
609
657
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80° N 78°
37 29
30
38
36
74°
33 17 42
72°
15
18 16
10a
W ¼ 0:0070L2:9750
for M: norvegica
(3) ðn ¼ 196; r 2 ¼ 0:994Þ
(4)
3. Results
2b
70°
for T: raschii
where W is the wet weight (mg) and L the length (mm). The biomass was obtained by multiplying the abundance by the individual weight of euphausiids in each sample. The obtained biomass was converted to dry weigh using a conversion factor 0.2 (Matthews and Heidal, 1980). The total number of samples collected in October–December 2004 and length measurements of each species individuals were taken into account (Anon, 1983). The calculations were done by fishery areas of the Barents Sea (Fig. 2).
35
76°
W ¼ 0:0020L3:4020
1961
13
3.1. Euphausiids distribution
68°
5°
10°
15°
20°
25°
30°
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45°
50°
55° E
Fig. 2. The regions of the Barents Sea, mentioned in the article. 2b—the northern slope of the Kanin-Kolguev Shallows; 10a—the north-eastern slope of the Murman Bank; 13—the Western Coastal area; 15—the Murman Tongue; 16—the Central Plateau; 17—the Demidov Bank; 18—the Central Deep; 29—the West Spitsbergen; 30—the South Cape Deep; 33—the Bear Island Bank Southern slope; 35—the Hopen Island area; 36—the Western Deep; 37—the Persey Elevation; 38—the Central Elevation; 42—the Kopytov area.
The results of the long-term investigations revealed interannual fluctuations of euphausiids abundance (Fig. 3). In 2000–2005, unusually large concentrations with density of 1000–5000 ind. m3 were observed both in the south-east and in the north-west of the Barents Sea (Fig. 4). Very dense (5000–56,000 ind. m3) local concentrations of euphausiids were recorded in the bathymetric range of 50–200 m depths. Mean annual index of euphausiids abundance exceeded the long-term
3.5
lg indices
3
2.5
2
1.5
1952 1956 1960 1964 1968 1972 1976 1980 1984 1988 1992 1996 2000 2004
3.5
lg indices
3 2.5 2 1.5 1
1952 1956 1960 1964 1968 1972 1976 1980 1984 1988 1992 1996 2000 2004 Years
Fig. 3. Changes of euphausiids abundance indices in the southern (A) and the north-western Barents Sea (B).
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60°
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70°
0°
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70° E
3
Fig. 4. Euphausiids distribution (ind. m
mean value by 1.5–3 times in 2000, 2002, 2003 and 2005, while in 2001 and 2004, it was close to this value. Thus, euphausiids were abundant in all these years.
3.2. Species composition in the south-eastern Barents Sea In the abnormally warm 2000, the high abundance of euphausiids (25,000–26,000 ind. m3) in the south-east Barents Sea were located in the depth range of 60–70 m (Fig. 4). T. raschii was the main component of the euphausiids population (65% of total euphausiids abundance), though euphausiids aggregations were heterogeneous and also included T. raschii and T. inermis (12% ) as well as M. norvegica (21%) (Fig. 5). Only very few individuals of T. longicaudata were recorded in the catches. In 2001, dense euphausiids aggregations (10,000–21,000 ind. m3) were observed further westwards than in 2000 and also
) in the Barents Sea in 2000–2005.
distributed deeper, at 100–150 m (Fig. 4). Unfortunately, there are no data on euphausiids species composition for this year. In 2002, T. raschii prevailed (57%) in the shallow areas (55–100 m), followed by T. inermis, T. longicaudata and M. norvegica by 40%, 2% and 1%, respectively (Fig. 5). In 2003, T. raschii was the dominating species (43%) in the bathymetric range of 60–120 m, while M. norvegica prevailed (42%) at depths of 100–150 m, while the proportion of T. inermis was up to 15% (Fig. 5). In 2004, dense aggregations of euphausiids at depth of 250 m consisted of T. inermis (57%), while in the layer 60–80 m, T. raschii dominated (47%) (Fig. 5). The relative abundance of M. norvegica was low (1%). In 2005, high abundance of euphausiids (6000–10,000 ind. m3) was recorded in the northern parts of the area. T. raschii was the main species there making up 60% of the euphausiids (Fig. 5), and T. inermis constituted 25%. The importance of the Atlantic
ARTICLE IN PRESS N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
1963
Fig. 5. Species composition of euphausiids in the south-eastern Barents Sea in 2000–2005.
species M. norvegica and T. longicaudata was low in these areas. Further south T. raschii prevailed (70%) at depths of 80–110 m (Fig. 5). In the south-east area of the sea with the dominance of T. raschii, three age groups of euphausiids were presented, namely recruits (age—0) 8–16 mm long, yearlings (age—1) 17–25 mm and 2-year olds (age—2) 26–28 mm, but their proportion was considerably different than in 2003 and 2004 (Fig. 7).
3.3. Species composition in the north-western Barents Sea In the north-western Barents Sea, T. inermis was the dominating species (75–98%) in the euphausiids aggregations, with densities exceeding 1000 ind. m3 (Figs. 4 and 6) during all years (2000–2005). The portions of T. raschii and T. longicaudata were approximately 10%, while the relative abundance of M. norvegica was 3% (Fig. 6). The length compositions of the populations were heterogeneous and consisted of a small number of young-of-the-years
9–14 mm long, yearlings 15–25 mm long (the bulk of the population), and 2-year olds 26–30 mm (Fig. 8). 3.4. Euphausiids biomass According to the results of biomass calculation, two areas with the maximal biomass were identified. One was in the north-west Barents Sea where biomasses of 1.7 g m2 in the Hopen area and 2.4 g m2 at Perseus Elevation, respectively, were found. The other area with high biomasses was located in the south-eastern Barents Sea (Fig. 9). T. inermis was the main species in all the samples from the first area, while T. inermis, T. raschii, M. norvegica dominated in the second area (Table 2).
4. Discussion The results on euphausiids species composition in the Barents Sea in the period from 2002 to 2005 confirmed the patterns
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Fig. 6. Species composition of euphausiids in the north-western Barents Sea in 2000–2005.
previously found (Nosova, 1970; Soboleva, 1973; Drobysheva, 1979, 1994; Filin et al., 2004). In the southern part of the Barents Sea, the relative inter-annual strength between the various euphausiids species may be linked to the changes in the seawater temperature. Thus in the warm 1950s–1960s, T. inermis constituted 40–70% of the total euphausiids abundance, while in the cold 1970s–1980s, it did not exceed 20–30% (Drobysheva, 1994). The abundance of T. raschii, another numerous species, changed in the opposite way, i.e. before 1970, its portion in euphausiids aggregations constituted 10–20%, and after 1970, it exceeded 50%. T. inermis was most important in 2000 and 2004, whereas T. raschii dominated in 2002 and 2003.
The portion of M. norvegica in total euphausiids abundance in the southern Barents Sea for the long-term period (1952–2005) was low and made up 5% on the average, although within the study period abundance of M. norvegica showed wide fluctuations. Thus, in the 1950s and early 1960s, the portion of M. norvegica was 10–20% (Drobysheva, 1994). From 1970 to 1983, no M. norvegica was caught during macro-plankton surveys, and only in 1984, 1988–1989, a few specimens were recorded (on the average about 1% of the total euphausiids abundance). In 1999–2000, the portion of M. norvegica in the southern Barents Sea increased again to the level of 1950s–1960s and constituted 18–26% (Drobysheva et al., 2003), and it was probably caused by the continuous increase in
ARTICLE IN PRESS N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
sea-water temperature during that period, since the abundance of this species depends on its advection by the Norwegian current. In the period 2000–2003 on the background of high water temperatures in the southern Barents Sea, a tendency toward decrease of water temperature was observed to the end of the period determining the inter-annual differences of the seasonal water temperature dynamics (Zhukova et al., 2006). In its turn, it influenced the species composition of euphausiids and
120 n=482
Abundance, ind.
100 80 60 40 20 0
8
10
12
14
16
18
20
22
24
26
28
M. norvegica in particular. Thus, in 2001, the decrease of M. norvegica abundance was observed, and in 2004–2005, in spite of these years being abnormally warm, its relative abundance remained low (7%). A very low abundance of this species even in years with high water temperature is probably caused by fish predation. M. norvegica is frequently found in cod fingerling stomachs and is a prey for adult cod as well (Ponomarenko and Yaragina, 1990; Pushchaeva, 1992). This large species (about 45 mm) is probably too big for capelin of 5–14 cm long, and thus capelin feed mainly on smaller euphausiids of Thysanoessa genus (18–20 mm). In 2003–2005, N. megalops, a moderate subtropical species, was found in the Barents Sea (Zhukova, 2006). This species was found in plankton samples from this water basin in the middle of last century, and its extreme eastern location was 681450 N, 381500 E (Zelikman, 1964). In 2003, N. megalops was found as far north-east as 731330 N, 521190 E and 731500 N, 501220 E. In October– December 2004–2005, the distribution of N. megalops was limited by the near-bottom 4.5 1C isotherm and only in the areas of the Atlantic waters invasion. The transference of N. megalops from its traditional habitats into the areas of high latitudes may be explained by the high advection of the Atlantic waters.
30
80° N
120
Abundance, ind.
1.4
78°
1.2
n=450
100
76°
80
1 0.8
60
74°
40
72°
0.6 0.4 0.2
20 0
1965
70°
8
10
12
14
16 18 20 22 Total length, mm
24
26
28
30
Fig. 7. Length frequency distribution of Thysanoessa raschii in the south-eastern Barents Sea in 2003 (A) and 2004 (B).
0
68° 10°
15°
20°
25°
30°
35°
40°
45°
400 n=2670
n=2942
300
Abundance, ind.
Abundance, ind.
55° E
Fig. 9. Euphausiids biomass distribution (g m2, dry weight) in October–December 2004.
400
200
100
0
50°
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16
18
20
22
24
26
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30
300
200
100
0
8
10
12
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16 18 20 22 Total length, mm
24
Fig. 8. Length frequency distribution of Thysanoessa inermis in the north-western Barents Sea in 2003 (A) and 2004 (B).
26
28
30
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Table 2 The biomass (g m2, dry weight) of the main euphausiids species in the Barents Sea in October–December 2004. Regions
Number of the region
T. inermis
T. longicaudata
T. raschii
M. norvegica
Total
The The The The The The The The The The The The The The The
29 35 30 33 37 36 38 42 18 15 16 17 10a 2b 13
0.7320 1.5499 1.0434 0.4243 2.3323 1.1204 1.0650 0.1005 0.3828 0.0750 0.0323 0.2530 0.8064 0.1959 0.0478
0.0154 0.0150 0.0025 0.0030 0.0308 0.0475 0.0150 0.0220 0.0062 0.0102 0.0001 0.0293 0.0023 – 0.0021
0.0464 0.0819 0.0149 – 0.0311 – 0.0431 – 0.0340 – 0.0069 – 0.0394 0.9348 0.0102
0.0604 0.0182 0.0025 0.2797 0.0661 0.4698 0.0768 0.1386 – 0.0249 0.0036 0.1162 0.0243 0.0048 0.4331
0.8542 1.6650 1.0633 0.7070 2.4603 1.6377 1.1999 0.2611 0.4230 0.1101 0.0429 0.3985 0.8724 1.1355 0.4932
West Spitsbergen Hopen Island area South Cape Deep Bear Island Bank Southern slope Persey Elevation Western Deep Central Elevation Kopytov area Central Deep Murman Tongue Central Plateau Demidov Bank north eastern slope of the Murman Bank northern slope of the Kanin-Kolguev Shallows Western Coastal area
Generally, in the south Barents Sea from 2000 to 2005, the species composition of euphausiids was heterogeneous as a result of both advected species from the Norwegian Sea (T. inermis, M. norvegica, T. longicaudata and N. megalops) and local reproduction of neritic species (T. raschii and T. inermis). T. inermis was the dominant species in the north-western Barents Sea in 2000–2005. Its adult specimens were limited by the 300-m isobath, while young individuals were found at 50 m depth. In 2004, in the area of 77–791N and 25–451E, euphausiids aggregations were found with the density of 41000 ind. m3 as well as local concentrations of 5000–7000 ind. m3. The highest contribution to these concentrations was made by the 20–30 mm length group of T. inermis at about 96% of the total abundance. The proportion of T. longicaudata (12–16 mm) and T. raschii (19–28 mm) constituted 2% each, respectively. T. raschii were less abundant in this area than in the southern sea. Mass spawning of T. raschii occurred in shallow waters in the south-eastern area. However, its nauplii were found in the Spitsbergen archipelago area (801N 301E), showing that their successful development is possible even in the area which is distant from native spawning grounds of this species (Timofeev, 1993). Sustainable concentrations of T. raschii in the SpitsbergenBear Island area appeared only in cold years (1960s–1970s); however, they were much smaller compared with the eastern concentrations (Drobysheva, 1988). According to earlier investigations (Drobysheva, 1979), a considerable amount of T. raschii was observed in the Spitsbergen bank in 1974–1976, whereas only single individuals were found in the surrounding deepwater areas. As T. longicaudata is an oceanic species, approximately 80% of which are concentrated offshore in the western part of the sea at depths over 200 m (Drobysheva, 1979). The minimal area of its distribution was observed in cold years, while the maximum area was registered after a series of warm years since the abundance of the species depends on the quantity of transferred individuals from the Norwegian Sea. In 1984–1992, a high abundance of T. longicaudata and T. inermis was found on the slope of the Spitsbergen bank (Dalpadado and Skjoldal, 1996). The population variation of the larger M. norvegica appears to be linked to the variations in the oceanography in a more complex way than that of the smaller species T. longicaudat. This may be due to the longer life span of the former, where the transfer time of M. norvegica from the main spawning grounds to the areas where the population are found with the 3-year age group will tend to decouple the effect of the ambient temperature on population growth and survival in the Barents Sea proper (Drobysheva et al., 2003). The high abundance of
M. norvegica is observed in the years preceded by warm periods, i.e. as a combined effect of oceanographic conditions of the 2–3 preceding years. We compared our data on euphausiids distribution with the same for warm period of 1989–1992. Dense concentrations of euphausiids (41000 ind. m3) in the mentioned years were found in the north-west area and the medium-size concentrations (101–1000 ind. m3) were observed in the south area. 1990 was an exception and dense concentrations of euphausiids (41000 ind. m3) were recorded in the Murmansk coastal areas. In 1989, 1991 and 1992, the mean annual indices of euphausiids abundance in the north-west of the sea were close to the longterm annual mean, while in 1990, this value was 4 times lower than the long-term mean. The southern part of the sea was not studied enough in 1990 and 1991, and, therefore, the mean annual abundance indices might be underestimated. However, in 1989 and 1992, they were 1.5–8 times lower than the long-term mean value. On the whole, the period of 1989–1992 belongs to the category of years with low euphausiids abundance. Probably, the main factor influencing the density of euphausiids concentrations in the years under study was the biotic factor, namely, grazing by capelin, the maximum stock of which was recorded in 1990–1992 with the minimum in 2003–2005 (PINRO, 2006). This assumption is proved by the high euphausiids abundance in cold 1986 and 1987 (in 1986, it exceeded the long-term mean value three times in the south of the sea) when the capelin stocks were low. The values of euphausiids biomass calculated based on the data of 2004 are similar to those by other researchers (Dalpadado and Skjoldal, 1991, 1996; Dalpadado et al., 1998; Timofeev, 2006), and the highest biomass was observed in the Arctic water masses in the north-western Barents Sea (Dalpadado and Skjoldal, 1991, 1996; Dalpadado et al., 1998). The differences in biomass values are mostly caused by seasonal and local variability and species composition of euphausiids.
5. Conclusions The recent long-lasting water warming has influenced the pattern of distribution of euphausiids in the Barents Sea. The distribution pattern of the main euphausiids aggregations are in accordance with general patterns of the distribution trends in warm years, where medium-size euphausiids concentrations (200–500 ind. m3) are found located in the coastal, central and partly in the western areas, while dense concentrations
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(41000 ind. m3) are observed in the south-east (Drobysheva, 1988). In the north-west Barents Sea, single, but dense euphausiids aggregations are formed in the central Spitsbergen bank and in the Hopen area. The total abundance of euphausiids in the Barents Sea is relatively stable in view of environmental changes, since euphausiids species with different zoogeographical characteristics tend to replace each other due to the prevailing climate conditions in the sea. The fluctuations of abundance in some species caused by change of water masses conditions only bring about re-distribution of euphausiids aggregations over the sea. Inter-annual variations of their abundance in the end of the year are mainly caused by the influence of the biotic factor, i.e. by predation. Acknowledgments We express our gratitude to Emma Orlova for her useful advice and correction of the manuscript and our colleagues from the Demersal Fish laboratory for collecting the samples. Our special thanks to the ECONORTH Symposium (Tromsø, March 2007) convenors Prof. Torstein Pedersen and Prof. Kurt Tande for the invitation and help while revising of the manuscript. References Anon, 1983. Modern methods of quantitative estimation of marine plankton. In: Vinogradov, M.E. (Ed.), Sovremennye metody kolichestvennoy otsenki morskogo planktona. Nauka, Moskva, 279pp. (in Russian). Brinton, E., Ohman, M.D., Townsend, A.W., Knight, M.D., Bridgeman, A.I., 1999. Euphausiids of the World Ocean. World Biodiversity Database CD-ROM Series. Expert Centre for Taxonomic Identifications (ETI). University of Amsterdam, Amsterdam. Dalpadado, P., Skjoldal, H.R., 1991. Distribution and life history of krill from the Barents Sea. Polar Research 10 (2), 443–460. Dalpadado, P., Skjoldal, H.R., 1996. Abundance, maturity and growth of krill species Thysanoessa inermis and T. longicaudata in the Barents Sea. Marine EcologyProgress Series 144, 175–183. Dalpadado, P., Ellertsen, B., Melle, W., Skjoldal, H.R., 1998. Summer distribution patterns and biomass estimates of macrozooplankton and micronecton in the Nordic Seas. Sarsia 83, 103–116. Drobysheva, S.S., 1957. The influence of some aspects of euphausiids biology on the feeding success of the Barents Sea cod (Vliyanie nekotorykh storon biologii Euphausiacea na usloviya letnego otkorma barentsevomorskoy treski) Murmansk. Trudy PINRO 10, 106–124 (in Russian). Drobysheva, S.S., 1979. Euphausiids formation in the Barents Sea (Formirovanie skopleniy evfausiid v Barentsevom more). Murmansk. Trudy PINRO 43, 54–76 (in Russian). Drobysheva, S.S., 1988. Reference data on long-term distribution areas of euphausiids being feeding grounds for commercial fishes in the Barents Sea (Spravochnyy material o mnogoletnem raspredelenii evfauziivykh rachkov— kormovykh zon promyslovykh rib Barents Sea). Izdatel’stvo PINRO, Murmansk, 128pp. (in Russian). Drobysheva, S.S., 1994. Euphausiids of the Barents Sea and their role for productivity. Evfausiidy Barentseva moray i ikh rol’ v formirovanii promyslovoy bioproduktsii. Izdatel’stvo PINRO, Murmansk, 139pp. (in Russian).
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Drobysheva, S.S., Timofeev, S.F., 1990. Euphausiids of the Barents Sea (Evfauziidy Barentseva moray). KNTS AN SSSR, Apatity, 33pp. (in Russian). Drobysheva, S.S., Nesterova, V.N., Nikiforov, A.G., Zhukova, N.G., 2003. The importance of warmwater species for local euphausiids assemblages in the south Barents Sea. (Rol’ teplovodnogo componenta v formirovanii lokal’nykh skopleniy evfauziid v yuzhnoy chasti Barentseva moray). Voprosy rybolovstva 4 2 (14), 209–216 (in Russian). Einarsson, H., 1945. Euphausiacea I. Northern Atlantic species. Dana Report 27 (Carlsberg Foundation), 185pp. Filin, A., Zhukova, N., Nesterova, V., 2004. Investigations by PINRO in the Spitsbergen Archipelago area. Issledovaniya PINRO v rayone arkhipelaga Shpitsbergen. Izdatel’stvo PINRO, Murmansk, pp. 82–90 (Chapter 4.2) (in Russian). Lomakina, N.B., 1978. Euphausiids of the World Ocean. Euphausiidy Mirovogo Oceana. Nauka Press, Leningrad, 224pp. (in Russian). Matthews, J.B.J., Heidal, B.R., 1980. Pelagic productivity and food chains in fjord system. In: Freelaand, H.S., Former, D.M., Levings, C.D. (Eds.), Fjord Oceanography. Plenum Press, New York, pp. 377–398. Nosova, E.K., 1970. Euphausiids distribution in the Barents Sea in 1967–1968 (Osobennosti raspredeleniya evfauziid v Barentsevom more osen’u i zimiy 1967–1968g). In: Materialy ribokhozyaystvennykh issledovaniy Severnogo basseyna, Murmansk, pp. 96–111 (in Russian). PINRO, A., 2006. Status of biological resources in the Barents Sea and the North Atlantic in 2006. Sostoyanie biologicheskikh syr’evykh resursov Barentseva morya i Severnoy Atlantiki na 2006 g. Izdatel’stvo PINRO, Murmansk, 99pp. (in Russian). Ponomarenko, I.Ya., Yaragina, N.A., 1990. Long-term dynamics of the Barents Sea cod predation on capelin, euphausiids and shrimp and their annual consumption (Mnogoletnyaya dinamika pitaniya treski Barentseva moray moyvoy, evfauziidami, krevetkoy i godovoe potreblenie etich ob’ektov). In: Kormovye resursy i pishchevye vzaimootnosheniyarib Severnoy Atlantiki. Sbornik nauchnykh trudov. Izdatel’stvo PINRO, Murmansk, pp. 109–130 (in Russian). Pushchaeva, T.Ya., 1992. Daily ration dynamics and trophical relationships of capelin and 0-group cod in autumn 1990 (Sutochnaya dynamika pitaniya i pishchevye vzaimootosheniya moyvy i segoletkov treski osen’yu 1990). In: Ekologicheskie problemy Barentseva morya. Sbornik nauchnykh trudov PINRO. Izdatel’stvo PINRO, Murmansk, pp. 200–224 (in Russian). Soboleva, M.S., 1973. The Role of Environmental Conditions for Euphausiids Abundance in North-Western Barents Sea (Rol’ abioticheskikh usloviy v formirovanii chislennosti evfauziid v severo-zapadnom rayone Barentseva moray). All-Union Conference on Marine and Oceanic Macroplankton, Moskva, 49pp. (in Russian). Timofeev, S.F., 1993. Zooplankton (definition, hierarchy, evolution, function), Zooplankton (opredelenie, ierarkhiya, evolutsiya, funktsiya). Apatity, 36pp. (in Russian). Timofeev, S.F., 2006. Euphausiids biomass in the Arctic Ocean. Crustaceana 79 (2), 157–165. Zelikman, E.A., 1958. Data on euphausiids reproduction in costal area of Murman, Materialy o raspredelenii i razmnozhenii evfauziid v pribrezhnoy zone Murmana. Trudy MBS 4, 79–117 (in Russian). Zelikman, E.A., 1964. Reproduction ecology of Euphausiacea mass species in the south-east Barents Sea, Ecologiya razmnozhenia massovykh vidov Euphausiacea v yugo-vostochnoy chasti Barentseva morya. Trudy MMBI 6, 12–21 (in Russian). Zhukova, N.G., 2006. On the distribution of Nematoscelis megalops (Crustacea, Euphausiacea) in the Barents Sea, K voprosu o rasprostranenii Nematoscelis megalops (Crustacea, Euphausiacea) v Barentsvom more. In: Materialy 10 nauchnoy konferentsii Belomorskoy biologicheskoy stantsii MGU im. N.M. Pertsova (9–10 Avgusta 2006). Grif i K. Moskva, pp. 109–111 (in Russian). Zhukova, N.G., Guzenko, V.V., Nesterova, V.N., 2006. Winter distribution of euphausiids aggregations in the Barents Sea in 2000–2003 and oceanographic factors determining it, Zimnee raspredelenie skopleniy evfauziid v Barentsevom more v 2000–2003 gg. i okeanographicheskye faktory, ego opredelyayushchie. Nauka I obrazovanie-2006. In: Materialy mezhdunarodnoy nauchno-technicheskoy konferentsii, Murmansk, pp. 684–689 (in Russian).
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Winter distribution of euphausiids (Euphausiacea) in the Barents Sea (2000–2005) Natalia G. Zhukova, Valentina N. Nesterova, Irina P. Prokopchuk , Galina B. Rudneva Polar Research Institute of Marine Fisheries and Oceanography (PINRO), 183038, 6 Knipovich Street, Murmansk, Russia
a r t i c l e in fo
abstract
Article history: Accepted 14 November 2008 Available online 3 December 2008
The purpose of the study is to analyze the state of the Barents Sea euphausiids populations in the warm period (2000–2005) based on the study of their structure dynamics and distribution under the influence of abiotic and biotic factors. For estimation of their aggregations in the bottom layer, the traditional method was used with the help of the modified egg net (0.2 m2 opening area, 564 mm mesh size). The net is used for collecting euphausiids in the autumn–winter period when their activity is reduced, which results in high-catch efficiency. The findings confirmed the major formation patterns of the euphausiids species composition associated with climate change in the Arctic basin. As before, in the warm years, one can see a clear-cut differentiation of space distribution of the dominant euphausiids Thysanoessa genus with localization of the more thermophilic Thysanoessa inermis in the north-west Barents Sea and Thysanoessa raschii in the east. The major euphausiids aggregations are formed of these species. In 2004, the first data of euphausiids distribution in the northern Barents Sea (77–791N) were obtained, and demonstrated extremely high concentrations of T. inermis in this area, with the biomass as high as 1.7–2.4 g m2 in terms of dry weight. These data have improved our knowledge of the distribution and euphausiids abundance during periods of elevated sea-water temperatures in the Barents Sea. The oceanic Atlantic species were found to increase in abundance due to elevated advection to the Barents Sea during the study period. Thus, after nearly a 30-year-long absence of the moderate subtropical Nematoscelis megalops in the Barents Sea, they were found again in 2003–2005. However in comparison with 1960, the north-east border of its distribution considerably shifted to 731500 N 501220 E. The portion of Meganyctiphanes norvegica also varied considerably—from 10% to 20% of the total euphausiids population in the warm 1950s–1960s almost to complete disappearing in 1970–1990s. The peak of this species’ occurrence (18–26%) took place in the beginning of warm period (1999–2000) after a succession of cold years. The subsequent reduction of the relative abundance of M. norvegica to 7% might have been mostly caused by fish predation during a period of low population densities of capelin. This high predation pressure may therefore have been mediated both by other pelagic fishes (i.e. herring, blue whiting, polar cod) but also by demersal fishes such as cod and haddock. Similar sharp fluctuations in the capelin stock (the major consumer of euphausiids) created marked perturbations in the food web in the Barents Sea in the middle 1980s and the early 1990s. & 2008 Elsevier Ltd. All rights reserved.
Keywords: Euphausiids Abundance Distribution Species composition Barents Sea
1. Introduction The fauna of euphausiids in the Barents Sea consists of six species. Thysanoessa inermis, Thysanoessa raschii and Meganyctiphanes norvegica are neritic species, whereas Thysanoessa longicaudata, Nematoscelis megalops and Stylocharion maximum are oceanic (Einarsson, 1945; Drobysheva, 1957, 1994; Lomakina, 1978; Brinton et al., 1999). The three species of Thysanoessa genus are zoogeographical characterized as arcto-boreal organisms, while M. norvegica is a boreal-arctic North-Atlantic species, N. megalops a moderate subtropical species, and S. maximum a
Corresponding author. Tel.: +7 8152 47 24 64; fax: +7 8152 47 33 31.
E-mail address: [email protected] (I.P. Prokopchuk). 0967-0645/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2008.11.007
moderate cold-water tropic species. T. inermis is distributed all over the Barents Sea, predominating in the western areas. T. raschii inhabits mainly the south-eastern shallows, while T. longicaudata is mostly associated with Atlantic waters. The distribution of M. norvegica is also limited by the Atlantic waters (Drobysheva, 1979, 1994; Dalpadado and Skjoldal, 1991, 1996). N. megalops and S. maximum are only rarely advected into the Barents Sea. Some authors (Zelikman, 1958; Drobysheva, 1994; Dalpadado and Skjoldal, 1991, 1996; Timofeev, 2006) estimate euphausiids biomass based on the length-to-weight relation. Euphausiids biomass is highly variable, and reflects local and inter-annual variations in growth conditions, birth, mortality and advection. It is difficult to assess the biomass variability and in particular to understand the underlying causes for these changes. Nevertheless, data are now available that enable us to provide a proxy of the
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entire euphausiids biomass for the Barents Sea, and demonstrate the regional difference for a particular time window. Russian survey data for euphausiids are now available for the years from 2001 to 2005, which is considered as a warm period in the Barents Sea. The objective of this study is to analyze the status of euphausiids population, to estimate their biomass, and thereby improve our understanding of the ecological role of euphausiids in the Barents Sea.
2. Material and methods Regular investigations of euphausiids in the Barents Sea have been carried out by PINRO since 1952. Macro-plankton, i.e. annual monitoring of abundance and distribution of euphausiids during
82° N 80°
78°
I
76° 74° II
72° 70° 68°
0°
10°
20°
30°
40°
50°
60°
70° E
Fig. 1. Location of plankton sampling stations in the Barents Sea in October– December 2000–2005: (I) The north-eastern Barents Sea and (II) the southern Barents Sea.
autumn–winter (October–December), were included in trawlacoustic surveys of demersal fishes in the Barents Sea. To collect macro-plankton a net (0.2-m2 opening area, 564-mm mesh size) was attached to the headline of a bottom trawl. Macro-plankton was thus sampled at 4–5 m above the bottom (the vertical opening of the bottom trawl). The autumn–winter period is the most effective for euphausiids sampling, as most of the species have reduced vertical migration and are found in more confined habitats at depths than what is true for the spring and summer period. Indices of euphausiids abundance (a number of individuals m3) were calculated by the net attached to trawl catches. In total, 1695 samples were processed in October–December 2000–2005 (Fig. 1, Table 1). A wide area from north of the Spitsbergen archipelago (801N, 101E) to the islands of the Novaya Zemlya and Kolguev (701N, 501E) was covered in the course of the surveys. In 2004, compared with the other years, the northern part of the Barents Sea was studied more thoroughly (791N, 30–401E). These investigated areas are the feeding grounds of both pelagic and demersal fish species. Species composition of euphausiids aggregations with a density of 41000 ind. m3 was studied in the north-western Barents Sea. This area is a core habitat for euphausiids where several species complete their entire life cycle (Drobysheva, 1979). The total length of euphausiid bodies was measured of the rostrum to the end of the telson (Einarsson, 1945). Separation of age groups (years 2002 and 2003 only) was based of length-age keys (Drobysheva, 1994). Biomass calculations were based on length (L) to weight (W) relationships for each of the three main euphausiid species (T. inermis, T. longicaudata, T. raschii) in the Barents Sea according to Eqs. (1)–(3) in Drobysheva and Timofeev (1990). For biomass of M. norvegica new length-to-weight relationships were used the following equation: W ¼ 0:0020L3:3640
for T: inermis
(1)
W ¼ 0:0048L3:0942
for T: longicaudata
(2)
Table 1 Abundance (ind. m3) of euphausiids in the Barents Sea. Year
Ship
Period
Number of stations
Southern Barents Sea
North-western Barents Sea
2000
AtlantNIRO Fridtjof Nansen
October 13–December 7 October 21–December 30
267
548
811
2001
AtlantNIRO Fridtjof Nansen
October 8–December 14 October 26–December 21
285
740
451
2002
Fridtjof Nansen Persey-3 Persey-3
October 16–December 29 November 16–December 8 January 29–March 03
249
1159
1354
2003
Smolensk Fridtjof Nansen G.O. Sars Smolensk
October 16–December 30 November 14–December 25 February 07–March 1 February 2–March 14
373
689
689
2004
Fridtjof Nansen Smolensk G.O. Sars Smolensk
October 13–December 28 October 14–December 29 February 7–March 7 February 9–March 3
318
464
501
2005
Fridtjof Nansen
October 23–December 15
203
609
657
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80° N 78°
37 29
30
38
36
74°
33 17 42
72°
15
18 16
10a
W ¼ 0:0070L2:9750
for M: norvegica
(3) ðn ¼ 196; r 2 ¼ 0:994Þ
(4)
3. Results
2b
70°
for T: raschii
where W is the wet weight (mg) and L the length (mm). The biomass was obtained by multiplying the abundance by the individual weight of euphausiids in each sample. The obtained biomass was converted to dry weigh using a conversion factor 0.2 (Matthews and Heidal, 1980). The total number of samples collected in October–December 2004 and length measurements of each species individuals were taken into account (Anon, 1983). The calculations were done by fishery areas of the Barents Sea (Fig. 2).
35
76°
W ¼ 0:0020L3:4020
1961
13
3.1. Euphausiids distribution
68°
5°
10°
15°
20°
25°
30°
35°
40°
45°
50°
55° E
Fig. 2. The regions of the Barents Sea, mentioned in the article. 2b—the northern slope of the Kanin-Kolguev Shallows; 10a—the north-eastern slope of the Murman Bank; 13—the Western Coastal area; 15—the Murman Tongue; 16—the Central Plateau; 17—the Demidov Bank; 18—the Central Deep; 29—the West Spitsbergen; 30—the South Cape Deep; 33—the Bear Island Bank Southern slope; 35—the Hopen Island area; 36—the Western Deep; 37—the Persey Elevation; 38—the Central Elevation; 42—the Kopytov area.
The results of the long-term investigations revealed interannual fluctuations of euphausiids abundance (Fig. 3). In 2000–2005, unusually large concentrations with density of 1000–5000 ind. m3 were observed both in the south-east and in the north-west of the Barents Sea (Fig. 4). Very dense (5000–56,000 ind. m3) local concentrations of euphausiids were recorded in the bathymetric range of 50–200 m depths. Mean annual index of euphausiids abundance exceeded the long-term
3.5
lg indices
3
2.5
2
1.5
1952 1956 1960 1964 1968 1972 1976 1980 1984 1988 1992 1996 2000 2004
3.5
lg indices
3 2.5 2 1.5 1
1952 1956 1960 1964 1968 1972 1976 1980 1984 1988 1992 1996 2000 2004 Years
Fig. 3. Changes of euphausiids abundance indices in the southern (A) and the north-western Barents Sea (B).
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N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
N 80°
80°
78°
78°
76°
76° 74°
74° 2000
72°
72°
70°
70°
68°
0°
10°
20°
30°
40°
50°
60°
68°
70°
80°
80°
78°
78°
76°
76°
74°
0°
10°
20°
30°
40°
50°
60°
70°
74° 2002
72°
2003
72°
70°
70°
68° 0°
10°
20°
30°
40°
50°
60°
68°
70°
80°
80°
78°
78°
76°
76°
74°
0°
10°
20°
30°
40°
50°
60°
70°
74° 2004
72°
2005
72°
70° 68°
2001
70° 0°
10°
20°
30°
40°
50°
60°
68°
70°
0°
10°
20°
30°
40°
50°
60°
70° E
3
Fig. 4. Euphausiids distribution (ind. m
mean value by 1.5–3 times in 2000, 2002, 2003 and 2005, while in 2001 and 2004, it was close to this value. Thus, euphausiids were abundant in all these years.
3.2. Species composition in the south-eastern Barents Sea In the abnormally warm 2000, the high abundance of euphausiids (25,000–26,000 ind. m3) in the south-east Barents Sea were located in the depth range of 60–70 m (Fig. 4). T. raschii was the main component of the euphausiids population (65% of total euphausiids abundance), though euphausiids aggregations were heterogeneous and also included T. raschii and T. inermis (12% ) as well as M. norvegica (21%) (Fig. 5). Only very few individuals of T. longicaudata were recorded in the catches. In 2001, dense euphausiids aggregations (10,000–21,000 ind. m3) were observed further westwards than in 2000 and also
) in the Barents Sea in 2000–2005.
distributed deeper, at 100–150 m (Fig. 4). Unfortunately, there are no data on euphausiids species composition for this year. In 2002, T. raschii prevailed (57%) in the shallow areas (55–100 m), followed by T. inermis, T. longicaudata and M. norvegica by 40%, 2% and 1%, respectively (Fig. 5). In 2003, T. raschii was the dominating species (43%) in the bathymetric range of 60–120 m, while M. norvegica prevailed (42%) at depths of 100–150 m, while the proportion of T. inermis was up to 15% (Fig. 5). In 2004, dense aggregations of euphausiids at depth of 250 m consisted of T. inermis (57%), while in the layer 60–80 m, T. raschii dominated (47%) (Fig. 5). The relative abundance of M. norvegica was low (1%). In 2005, high abundance of euphausiids (6000–10,000 ind. m3) was recorded in the northern parts of the area. T. raschii was the main species there making up 60% of the euphausiids (Fig. 5), and T. inermis constituted 25%. The importance of the Atlantic
ARTICLE IN PRESS N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
1963
Fig. 5. Species composition of euphausiids in the south-eastern Barents Sea in 2000–2005.
species M. norvegica and T. longicaudata was low in these areas. Further south T. raschii prevailed (70%) at depths of 80–110 m (Fig. 5). In the south-east area of the sea with the dominance of T. raschii, three age groups of euphausiids were presented, namely recruits (age—0) 8–16 mm long, yearlings (age—1) 17–25 mm and 2-year olds (age—2) 26–28 mm, but their proportion was considerably different than in 2003 and 2004 (Fig. 7).
3.3. Species composition in the north-western Barents Sea In the north-western Barents Sea, T. inermis was the dominating species (75–98%) in the euphausiids aggregations, with densities exceeding 1000 ind. m3 (Figs. 4 and 6) during all years (2000–2005). The portions of T. raschii and T. longicaudata were approximately 10%, while the relative abundance of M. norvegica was 3% (Fig. 6). The length compositions of the populations were heterogeneous and consisted of a small number of young-of-the-years
9–14 mm long, yearlings 15–25 mm long (the bulk of the population), and 2-year olds 26–30 mm (Fig. 8). 3.4. Euphausiids biomass According to the results of biomass calculation, two areas with the maximal biomass were identified. One was in the north-west Barents Sea where biomasses of 1.7 g m2 in the Hopen area and 2.4 g m2 at Perseus Elevation, respectively, were found. The other area with high biomasses was located in the south-eastern Barents Sea (Fig. 9). T. inermis was the main species in all the samples from the first area, while T. inermis, T. raschii, M. norvegica dominated in the second area (Table 2).
4. Discussion The results on euphausiids species composition in the Barents Sea in the period from 2002 to 2005 confirmed the patterns
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N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
Fig. 6. Species composition of euphausiids in the north-western Barents Sea in 2000–2005.
previously found (Nosova, 1970; Soboleva, 1973; Drobysheva, 1979, 1994; Filin et al., 2004). In the southern part of the Barents Sea, the relative inter-annual strength between the various euphausiids species may be linked to the changes in the seawater temperature. Thus in the warm 1950s–1960s, T. inermis constituted 40–70% of the total euphausiids abundance, while in the cold 1970s–1980s, it did not exceed 20–30% (Drobysheva, 1994). The abundance of T. raschii, another numerous species, changed in the opposite way, i.e. before 1970, its portion in euphausiids aggregations constituted 10–20%, and after 1970, it exceeded 50%. T. inermis was most important in 2000 and 2004, whereas T. raschii dominated in 2002 and 2003.
The portion of M. norvegica in total euphausiids abundance in the southern Barents Sea for the long-term period (1952–2005) was low and made up 5% on the average, although within the study period abundance of M. norvegica showed wide fluctuations. Thus, in the 1950s and early 1960s, the portion of M. norvegica was 10–20% (Drobysheva, 1994). From 1970 to 1983, no M. norvegica was caught during macro-plankton surveys, and only in 1984, 1988–1989, a few specimens were recorded (on the average about 1% of the total euphausiids abundance). In 1999–2000, the portion of M. norvegica in the southern Barents Sea increased again to the level of 1950s–1960s and constituted 18–26% (Drobysheva et al., 2003), and it was probably caused by the continuous increase in
ARTICLE IN PRESS N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
sea-water temperature during that period, since the abundance of this species depends on its advection by the Norwegian current. In the period 2000–2003 on the background of high water temperatures in the southern Barents Sea, a tendency toward decrease of water temperature was observed to the end of the period determining the inter-annual differences of the seasonal water temperature dynamics (Zhukova et al., 2006). In its turn, it influenced the species composition of euphausiids and
120 n=482
Abundance, ind.
100 80 60 40 20 0
8
10
12
14
16
18
20
22
24
26
28
M. norvegica in particular. Thus, in 2001, the decrease of M. norvegica abundance was observed, and in 2004–2005, in spite of these years being abnormally warm, its relative abundance remained low (7%). A very low abundance of this species even in years with high water temperature is probably caused by fish predation. M. norvegica is frequently found in cod fingerling stomachs and is a prey for adult cod as well (Ponomarenko and Yaragina, 1990; Pushchaeva, 1992). This large species (about 45 mm) is probably too big for capelin of 5–14 cm long, and thus capelin feed mainly on smaller euphausiids of Thysanoessa genus (18–20 mm). In 2003–2005, N. megalops, a moderate subtropical species, was found in the Barents Sea (Zhukova, 2006). This species was found in plankton samples from this water basin in the middle of last century, and its extreme eastern location was 681450 N, 381500 E (Zelikman, 1964). In 2003, N. megalops was found as far north-east as 731330 N, 521190 E and 731500 N, 501220 E. In October– December 2004–2005, the distribution of N. megalops was limited by the near-bottom 4.5 1C isotherm and only in the areas of the Atlantic waters invasion. The transference of N. megalops from its traditional habitats into the areas of high latitudes may be explained by the high advection of the Atlantic waters.
30
80° N
120
Abundance, ind.
1.4
78°
1.2
n=450
100
76°
80
1 0.8
60
74°
40
72°
0.6 0.4 0.2
20 0
1965
70°
8
10
12
14
16 18 20 22 Total length, mm
24
26
28
30
Fig. 7. Length frequency distribution of Thysanoessa raschii in the south-eastern Barents Sea in 2003 (A) and 2004 (B).
0
68° 10°
15°
20°
25°
30°
35°
40°
45°
400 n=2670
n=2942
300
Abundance, ind.
Abundance, ind.
55° E
Fig. 9. Euphausiids biomass distribution (g m2, dry weight) in October–December 2004.
400
200
100
0
50°
8
10
12
14
16
18
20
22
24
26
28
30
300
200
100
0
8
10
12
14
16 18 20 22 Total length, mm
24
Fig. 8. Length frequency distribution of Thysanoessa inermis in the north-western Barents Sea in 2003 (A) and 2004 (B).
26
28
30
ARTICLE IN PRESS 1966
N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
Table 2 The biomass (g m2, dry weight) of the main euphausiids species in the Barents Sea in October–December 2004. Regions
Number of the region
T. inermis
T. longicaudata
T. raschii
M. norvegica
Total
The The The The The The The The The The The The The The The
29 35 30 33 37 36 38 42 18 15 16 17 10a 2b 13
0.7320 1.5499 1.0434 0.4243 2.3323 1.1204 1.0650 0.1005 0.3828 0.0750 0.0323 0.2530 0.8064 0.1959 0.0478
0.0154 0.0150 0.0025 0.0030 0.0308 0.0475 0.0150 0.0220 0.0062 0.0102 0.0001 0.0293 0.0023 – 0.0021
0.0464 0.0819 0.0149 – 0.0311 – 0.0431 – 0.0340 – 0.0069 – 0.0394 0.9348 0.0102
0.0604 0.0182 0.0025 0.2797 0.0661 0.4698 0.0768 0.1386 – 0.0249 0.0036 0.1162 0.0243 0.0048 0.4331
0.8542 1.6650 1.0633 0.7070 2.4603 1.6377 1.1999 0.2611 0.4230 0.1101 0.0429 0.3985 0.8724 1.1355 0.4932
West Spitsbergen Hopen Island area South Cape Deep Bear Island Bank Southern slope Persey Elevation Western Deep Central Elevation Kopytov area Central Deep Murman Tongue Central Plateau Demidov Bank north eastern slope of the Murman Bank northern slope of the Kanin-Kolguev Shallows Western Coastal area
Generally, in the south Barents Sea from 2000 to 2005, the species composition of euphausiids was heterogeneous as a result of both advected species from the Norwegian Sea (T. inermis, M. norvegica, T. longicaudata and N. megalops) and local reproduction of neritic species (T. raschii and T. inermis). T. inermis was the dominant species in the north-western Barents Sea in 2000–2005. Its adult specimens were limited by the 300-m isobath, while young individuals were found at 50 m depth. In 2004, in the area of 77–791N and 25–451E, euphausiids aggregations were found with the density of 41000 ind. m3 as well as local concentrations of 5000–7000 ind. m3. The highest contribution to these concentrations was made by the 20–30 mm length group of T. inermis at about 96% of the total abundance. The proportion of T. longicaudata (12–16 mm) and T. raschii (19–28 mm) constituted 2% each, respectively. T. raschii were less abundant in this area than in the southern sea. Mass spawning of T. raschii occurred in shallow waters in the south-eastern area. However, its nauplii were found in the Spitsbergen archipelago area (801N 301E), showing that their successful development is possible even in the area which is distant from native spawning grounds of this species (Timofeev, 1993). Sustainable concentrations of T. raschii in the SpitsbergenBear Island area appeared only in cold years (1960s–1970s); however, they were much smaller compared with the eastern concentrations (Drobysheva, 1988). According to earlier investigations (Drobysheva, 1979), a considerable amount of T. raschii was observed in the Spitsbergen bank in 1974–1976, whereas only single individuals were found in the surrounding deepwater areas. As T. longicaudata is an oceanic species, approximately 80% of which are concentrated offshore in the western part of the sea at depths over 200 m (Drobysheva, 1979). The minimal area of its distribution was observed in cold years, while the maximum area was registered after a series of warm years since the abundance of the species depends on the quantity of transferred individuals from the Norwegian Sea. In 1984–1992, a high abundance of T. longicaudata and T. inermis was found on the slope of the Spitsbergen bank (Dalpadado and Skjoldal, 1996). The population variation of the larger M. norvegica appears to be linked to the variations in the oceanography in a more complex way than that of the smaller species T. longicaudat. This may be due to the longer life span of the former, where the transfer time of M. norvegica from the main spawning grounds to the areas where the population are found with the 3-year age group will tend to decouple the effect of the ambient temperature on population growth and survival in the Barents Sea proper (Drobysheva et al., 2003). The high abundance of
M. norvegica is observed in the years preceded by warm periods, i.e. as a combined effect of oceanographic conditions of the 2–3 preceding years. We compared our data on euphausiids distribution with the same for warm period of 1989–1992. Dense concentrations of euphausiids (41000 ind. m3) in the mentioned years were found in the north-west area and the medium-size concentrations (101–1000 ind. m3) were observed in the south area. 1990 was an exception and dense concentrations of euphausiids (41000 ind. m3) were recorded in the Murmansk coastal areas. In 1989, 1991 and 1992, the mean annual indices of euphausiids abundance in the north-west of the sea were close to the longterm annual mean, while in 1990, this value was 4 times lower than the long-term mean. The southern part of the sea was not studied enough in 1990 and 1991, and, therefore, the mean annual abundance indices might be underestimated. However, in 1989 and 1992, they were 1.5–8 times lower than the long-term mean value. On the whole, the period of 1989–1992 belongs to the category of years with low euphausiids abundance. Probably, the main factor influencing the density of euphausiids concentrations in the years under study was the biotic factor, namely, grazing by capelin, the maximum stock of which was recorded in 1990–1992 with the minimum in 2003–2005 (PINRO, 2006). This assumption is proved by the high euphausiids abundance in cold 1986 and 1987 (in 1986, it exceeded the long-term mean value three times in the south of the sea) when the capelin stocks were low. The values of euphausiids biomass calculated based on the data of 2004 are similar to those by other researchers (Dalpadado and Skjoldal, 1991, 1996; Dalpadado et al., 1998; Timofeev, 2006), and the highest biomass was observed in the Arctic water masses in the north-western Barents Sea (Dalpadado and Skjoldal, 1991, 1996; Dalpadado et al., 1998). The differences in biomass values are mostly caused by seasonal and local variability and species composition of euphausiids.
5. Conclusions The recent long-lasting water warming has influenced the pattern of distribution of euphausiids in the Barents Sea. The distribution pattern of the main euphausiids aggregations are in accordance with general patterns of the distribution trends in warm years, where medium-size euphausiids concentrations (200–500 ind. m3) are found located in the coastal, central and partly in the western areas, while dense concentrations
ARTICLE IN PRESS N.G. Zhukova et al. / Deep-Sea Research II 56 (2009) 1959–1967
(41000 ind. m3) are observed in the south-east (Drobysheva, 1988). In the north-west Barents Sea, single, but dense euphausiids aggregations are formed in the central Spitsbergen bank and in the Hopen area. The total abundance of euphausiids in the Barents Sea is relatively stable in view of environmental changes, since euphausiids species with different zoogeographical characteristics tend to replace each other due to the prevailing climate conditions in the sea. The fluctuations of abundance in some species caused by change of water masses conditions only bring about re-distribution of euphausiids aggregations over the sea. Inter-annual variations of their abundance in the end of the year are mainly caused by the influence of the biotic factor, i.e. by predation. Acknowledgments We express our gratitude to Emma Orlova for her useful advice and correction of the manuscript and our colleagues from the Demersal Fish laboratory for collecting the samples. Our special thanks to the ECONORTH Symposium (Tromsø, March 2007) convenors Prof. Torstein Pedersen and Prof. Kurt Tande for the invitation and help while revising of the manuscript. References Anon, 1983. Modern methods of quantitative estimation of marine plankton. In: Vinogradov, M.E. (Ed.), Sovremennye metody kolichestvennoy otsenki morskogo planktona. Nauka, Moskva, 279pp. (in Russian). Brinton, E., Ohman, M.D., Townsend, A.W., Knight, M.D., Bridgeman, A.I., 1999. Euphausiids of the World Ocean. World Biodiversity Database CD-ROM Series. Expert Centre for Taxonomic Identifications (ETI). University of Amsterdam, Amsterdam. Dalpadado, P., Skjoldal, H.R., 1991. Distribution and life history of krill from the Barents Sea. Polar Research 10 (2), 443–460. Dalpadado, P., Skjoldal, H.R., 1996. Abundance, maturity and growth of krill species Thysanoessa inermis and T. longicaudata in the Barents Sea. Marine EcologyProgress Series 144, 175–183. Dalpadado, P., Ellertsen, B., Melle, W., Skjoldal, H.R., 1998. Summer distribution patterns and biomass estimates of macrozooplankton and micronecton in the Nordic Seas. Sarsia 83, 103–116. Drobysheva, S.S., 1957. The influence of some aspects of euphausiids biology on the feeding success of the Barents Sea cod (Vliyanie nekotorykh storon biologii Euphausiacea na usloviya letnego otkorma barentsevomorskoy treski) Murmansk. Trudy PINRO 10, 106–124 (in Russian). Drobysheva, S.S., 1979. Euphausiids formation in the Barents Sea (Formirovanie skopleniy evfausiid v Barentsevom more). Murmansk. Trudy PINRO 43, 54–76 (in Russian). Drobysheva, S.S., 1988. Reference data on long-term distribution areas of euphausiids being feeding grounds for commercial fishes in the Barents Sea (Spravochnyy material o mnogoletnem raspredelenii evfauziivykh rachkov— kormovykh zon promyslovykh rib Barents Sea). Izdatel’stvo PINRO, Murmansk, 128pp. (in Russian). Drobysheva, S.S., 1994. Euphausiids of the Barents Sea and their role for productivity. Evfausiidy Barentseva moray i ikh rol’ v formirovanii promyslovoy bioproduktsii. Izdatel’stvo PINRO, Murmansk, 139pp. (in Russian).
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Drobysheva, S.S., Timofeev, S.F., 1990. Euphausiids of the Barents Sea (Evfauziidy Barentseva moray). KNTS AN SSSR, Apatity, 33pp. (in Russian). Drobysheva, S.S., Nesterova, V.N., Nikiforov, A.G., Zhukova, N.G., 2003. The importance of warmwater species for local euphausiids assemblages in the south Barents Sea. (Rol’ teplovodnogo componenta v formirovanii lokal’nykh skopleniy evfauziid v yuzhnoy chasti Barentseva moray). Voprosy rybolovstva 4 2 (14), 209–216 (in Russian). Einarsson, H., 1945. Euphausiacea I. Northern Atlantic species. Dana Report 27 (Carlsberg Foundation), 185pp. Filin, A., Zhukova, N., Nesterova, V., 2004. Investigations by PINRO in the Spitsbergen Archipelago area. Issledovaniya PINRO v rayone arkhipelaga Shpitsbergen. Izdatel’stvo PINRO, Murmansk, pp. 82–90 (Chapter 4.2) (in Russian). Lomakina, N.B., 1978. Euphausiids of the World Ocean. Euphausiidy Mirovogo Oceana. Nauka Press, Leningrad, 224pp. (in Russian). Matthews, J.B.J., Heidal, B.R., 1980. Pelagic productivity and food chains in fjord system. In: Freelaand, H.S., Former, D.M., Levings, C.D. (Eds.), Fjord Oceanography. Plenum Press, New York, pp. 377–398. Nosova, E.K., 1970. Euphausiids distribution in the Barents Sea in 1967–1968 (Osobennosti raspredeleniya evfauziid v Barentsevom more osen’u i zimiy 1967–1968g). In: Materialy ribokhozyaystvennykh issledovaniy Severnogo basseyna, Murmansk, pp. 96–111 (in Russian). PINRO, A., 2006. Status of biological resources in the Barents Sea and the North Atlantic in 2006. Sostoyanie biologicheskikh syr’evykh resursov Barentseva morya i Severnoy Atlantiki na 2006 g. Izdatel’stvo PINRO, Murmansk, 99pp. (in Russian). Ponomarenko, I.Ya., Yaragina, N.A., 1990. Long-term dynamics of the Barents Sea cod predation on capelin, euphausiids and shrimp and their annual consumption (Mnogoletnyaya dinamika pitaniya treski Barentseva moray moyvoy, evfauziidami, krevetkoy i godovoe potreblenie etich ob’ektov). In: Kormovye resursy i pishchevye vzaimootnosheniyarib Severnoy Atlantiki. Sbornik nauchnykh trudov. Izdatel’stvo PINRO, Murmansk, pp. 109–130 (in Russian). Pushchaeva, T.Ya., 1992. Daily ration dynamics and trophical relationships of capelin and 0-group cod in autumn 1990 (Sutochnaya dynamika pitaniya i pishchevye vzaimootosheniya moyvy i segoletkov treski osen’yu 1990). In: Ekologicheskie problemy Barentseva morya. Sbornik nauchnykh trudov PINRO. Izdatel’stvo PINRO, Murmansk, pp. 200–224 (in Russian). Soboleva, M.S., 1973. The Role of Environmental Conditions for Euphausiids Abundance in North-Western Barents Sea (Rol’ abioticheskikh usloviy v formirovanii chislennosti evfauziid v severo-zapadnom rayone Barentseva moray). All-Union Conference on Marine and Oceanic Macroplankton, Moskva, 49pp. (in Russian). Timofeev, S.F., 1993. Zooplankton (definition, hierarchy, evolution, function), Zooplankton (opredelenie, ierarkhiya, evolutsiya, funktsiya). Apatity, 36pp. (in Russian). Timofeev, S.F., 2006. Euphausiids biomass in the Arctic Ocean. Crustaceana 79 (2), 157–165. Zelikman, E.A., 1958. Data on euphausiids reproduction in costal area of Murman, Materialy o raspredelenii i razmnozhenii evfauziid v pribrezhnoy zone Murmana. Trudy MBS 4, 79–117 (in Russian). Zelikman, E.A., 1964. Reproduction ecology of Euphausiacea mass species in the south-east Barents Sea, Ecologiya razmnozhenia massovykh vidov Euphausiacea v yugo-vostochnoy chasti Barentseva morya. Trudy MMBI 6, 12–21 (in Russian). Zhukova, N.G., 2006. On the distribution of Nematoscelis megalops (Crustacea, Euphausiacea) in the Barents Sea, K voprosu o rasprostranenii Nematoscelis megalops (Crustacea, Euphausiacea) v Barentsvom more. In: Materialy 10 nauchnoy konferentsii Belomorskoy biologicheskoy stantsii MGU im. N.M. Pertsova (9–10 Avgusta 2006). Grif i K. Moskva, pp. 109–111 (in Russian). Zhukova, N.G., Guzenko, V.V., Nesterova, V.N., 2006. Winter distribution of euphausiids aggregations in the Barents Sea in 2000–2003 and oceanographic factors determining it, Zimnee raspredelenie skopleniy evfauziid v Barentsevom more v 2000–2003 gg. i okeanographicheskye faktory, ego opredelyayushchie. Nauka I obrazovanie-2006. In: Materialy mezhdunarodnoy nauchno-technicheskoy konferentsii, Murmansk, pp. 684–689 (in Russian).