Dramatic Declines in Euphausia pacifica Abundance in the East China Sea: Response to Recent Regional Climate Change Author(s): Zhao-Li Xu and Dong Zhang Source: Zoological Science, 31(3):135-142. 2014. Published By: Zoological Society of Japan DOI: http://dx.doi.org/10.2108/zsj.31.135 URL: http://www.bioone.org/doi/full/10.2108/zsj.31.135
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
¤ 2014 Zoological Society of Japan
ZOOLOGICAL SCIENCE 31: 135–142 (2014)
Dramatic Declines in Euphausia pacifica Abundance in the East China Sea: Response to Recent Regional Climate Change Zhao-Li Xu and Dong Zhang* East China Sea Fisheries Research Institute, Chinese Academy of Fisheries Science, Jun Gong Road, Shanghai 200090, China
As with other marine ecosystems around the world, water temperature has been anomalously warm in recent years in the East China Sea. We analyzed historical data to explore the effects of climatic change on the abundance and distribution variation of Euphausia pacifica in the East China Sea (the Changjiang River estuary and adjacent areas). In 1959, the highest abundance occurred in the spring and autumn, and this krill species was still abundant in May 1974; however, its abundance was significantly reduced in 2002, markedly in spring. Euphausia pacifica was the numerically dominant euphausiid in the East China Sea in 1959. Its mean abundance was up to 1.91 ind m–3 and 1.64 ind/m3 in 1959 and 1974, respectively; however, this figure decreased to 0.36 ind m–3 in 2002. Since 2003, the abundances have been near zero in the most years. Both inter-annual (between November 1959 and 2002) and inter-monthly (between May and June 1959) comparisons suggest that E. pacifica has had a temperature-driven northward movement in response to rising sea surface temperature, especially the positive anomalies since 1997. However, E. pacifica did not come back to the previous habitat when temperature became relative cold. Hence additional factors affecting the E. pacifica distribution and abundance need to be investigated in the future study. Key words: Euphausia pacifica, global warming, abundance, distribution shift, East China Sea, temperature anomaly INTRODUCTION The effects of climate change on species and communities can be examined through physiological changes, distributions, phenology, and regional adaptations (Hughes, 2000). Modification of the distribution range of pelagic organisms is a sensitive and well-documented indicator of climate change (e.g., Beaugrand et al., 2002; Perry et al., 2005; Greenstein and Pandolfi, 2008). How global climate change might affect phytoplankton is a marked concern because they play a fundamental role in the food web by providing half the global primary production (Falkowski et al., 1998; Boyce et al., 2010). Many studies have explored the impact of climatic change on zooplankton biomass and community structure across distinct geographic regions, such as California coastal waters (Roemmich and McGowan, 1995; Rebstock, 2002; Brinton and Townsand, 2003), the Northern Baltic Archipelago Sea (Dippner et al., 2001), North Atlantic (Beaugrand et al., 2002; Beaugrand and Reid, 2003), Northeast Atlantic (Richardson and Schoeman, 2004), subarctic North Pacific (Chiba et al., 2006), and the Northwestern Mediterranean Sea (Molinero et al., 2008). Responses of zooplankton to temperature variability vary regionally depending on community structure and local oceanographic conditions. For example, the krill-like Euphausia pacifica shrinks (Marinovic and Mangel, 1999) * Corresponding author. Tel. : +86-21-65684655; Fax : +86-21-65683926; E-mail : [email protected] doi:10.2108/zsj.31.135
and decrease its brood sizes (Gómez-Gutiérrez et al., 2007) and egg hatch success (Iguchi and Ikeda, 1994) in response to elevated water temperatures. Distribution shift and species composition change are likely the most immediate responses to regional climate change in the pelagic ecosystem (Tanasichuk, 1998; Mackas et al., 2001; Beaugrand et al., 2002). Compared with the extensive zooplankton sampling effort in California Current System, we do not understand how climate change impacts on the marine ecosystem of the Western Pacific, especially off the Chinese coastal waters, due to comparatively limited information to date obtained. In the present study, we investigated the interannual temperature impact on the krill species E. pacifica in the East China Sea (the Changjiang River estuary and adjacent area). The East China Sea is greatly influenced by the runoff from the Changjiang River, the Yellow Sea Coastal Current and the Taiwan Current (Su and Yuan, 2005). There is no evident stratification season in the East China Sea, especially in the area studied (Su and Yuan, 2005). This area is one of the most productive waters in the world due to nutrient runoffs from the Changjiang River and provides spawning and nursery grounds for numerous species of pelagic fish species (Chen and Shen, 1999; Tu and Wang, 2006). Understanding the effect of global climate change on plankton communities is essential to regulate the fisheries’ resource exploitation and management from this region of China. Euphausia pacifica is the dominant euphausiid species in the East China Sea, being the only Euphausia species with temperate zoogeographic distribution in the North Pacific (Brinton, 1962). It is considered one of the key zoo-
136
Z.-L. Xu and D. Zhang
plankton species in the food web of the northwestern Pacific, serving as prey for many endemic and migrant fish species, marine mammals, and sea birds (Nemoto, 1957; Ogi and Tanaka, 1984; Tanasichuk et al., 1991; Yamamura et al., 1998). Euphausia pacifica is mainly distributed in the Yellow Sea in China (Cai, 1986). In the East China Sea, E. pacifica is mainly distributed in the Changjiang estuary and adjacent areas (29–32°N, 121.5–123.5°E), with high abundance in the spring and autumn (Xu, 2007). The spatial and temporal distribution of E. pacifica in the Yellow Sea and East China Sea is significantly affected by the Yellow Sea Bottom Cold Water (YSBCW) which offers the species a refuge from warm surface water in summer and autumn (Cai, 1986; Sun et al., 2011), The spatial distribution of the species is primarily controlled by seawater temperature (Yoon et al., 2000; Sun et al., 2011). Thus this species may also be a sensitive indicator of regional sea warming, as several reports have shown significant abundance changes of E. pacifica off the coast of California and Baja California after the 1976 climate regime (Gómez-Gutiérrez et al., 1995; Linacre, 2004; Lavaniegos and Ohman, 2007). We studied E. pacifica to examine the effects of climate change occurred between 1959 and 2012 in the East China Sea. We analyzed historical data to explore the effects of temperature increase on abundance and distribution patterns of E. pacifica in the Changjiang estuary and adjacent areas. MATERIALS AND METHODS
bottom salinity (SS and BS) were recorded at each sampling site with an SBE-19 CTD, except in 1959 and 1974 when surface and seafloor temperature was measured with a simplified reversing thermometer, and salinity was determined with hydrometer. Bottom depths of the sampling sites were 40–200 m, but mostly collected at 50–100 m depth. To show temperature trend, sea surface temperatures recorded in May of 1971–2011 with the satellite AVHRR in area between 28°30′–32°00′N and 121°30′–123°30′E were obtained. This allows us to study long-term anomalous temperature change. Data analysis We made a comparison of Euphausia pacifica abundance (ind.m–3) and distribution change using data collected in 1959 and 2002–2012. Seasonal comparisons were done using data from 1959 and 2002. Data from spring of 1959 and 2002, and 1959 and 2005 were also compared. Euphausia pacifica relative occurrence is shown as the percentage of stations where this species was present over the entire region. Mean values of abundances and temperatures were initially tested for normality and homogeneity of variance and then Duncan multiple comparisons was applied to test significance of interannual difference in mean E. pacifica abundances and temperatures. Statistical analyses were performed using SPSS 11.5.
RESULTS Interannual variation of temperature in spring In the East China Sea, ST and BT in May of recent years (except ST in 2004, 2006, 2008, and 2010, and BT in 2004, 2006, and 2010 years), were significantly higher (Duncan multiple test, P < 0.05) than those in 1959 (Table 1). Sea surface temperature (satellite data) in the East China Sea was generally below average before 1997 (temperatures in only four of 26 years were above average, 18.33°C), followed by a marked upward pattern from 1997
Study area and sampling To assess the abundance and distribution of Euphausia pacifica, we collected zooplankton samples between 29°00′–32°00′N and 122°00′–123°30′E (Fig. 1). In 1959, data were obtained from collections made in the winter (February), spring (from March to June), summer (August), and autumn (November). In 2002, data were collected in the winter (February), spring (May), summer (August), and autumn (November). From 2003 to 2012, the surveys were conducted only in the spring (May). Three additional surveys were conducted in March, April, and June of 2005. Moreover, data collected at six stations in the area in May 1974 were also presented, as supplemental evidence. Euphausiids were sampled during the day in all years by towing a zooplankton net with an 80-cm diameter mouth and 505-μm mesh vertically from near the bottom to the surface. The volume of water filtered was measured with a flow meter mounted at the net mouth. Abundance (ind.m–3) was estimated from water volume filtered and the mean for all sampling stations was calculated. For comparison purposes data collected at the same stations for each year over the years were used to estimate mean E. pacifica abundance. For example 27 sampling stations were selected to compare mean abundance between 1959 and the 2002–2012 period, and 40 sampling stations to compare mean abundance in February–June of 1959 (Fig. 1). The samples were immediately preserved in 5% formalin buffered with Sodium Fig. 1. Map of sampling stations. (A) sampling stations both in 1959 and 2002–2012, and borate. Surface (ST) and bottom (BT) temsix sampling stations in 1974; (B) sampling stations in 1959 (see Materials and Methods for perature (5 m from bottom), and surface and details).
Declines in Euphausia pacifica abundance Table 1. Surface temperature (ST), bottom temperature (BT), surface salinity (SS), bottom salinity (BS), abundance (A), and occurrence (O) in May 1959, 1974 and 2002–2012 (mean ± s.e., n = 27). Year
ST (°C)
BT (°C)
SS
BS
A (ind.m–3)
O (%)
1959 1974 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
17.86 ± 0.21b 17.40 ± 0.22 19.53 ± 0.20a 18.95 ± 0.23a 18.34 ± 0.21b 18.94 ± 0.30a 18.51 ± 0.35b 19.94 ± 0.27a 18.63 ± 0.16b 20.90 ± 0.29a 17.84 ± 0.29b 19.03 ± 0.25a 18.67 ± 0.22b
17.08 ± 0.32b 17.12 ± 0.21 19.58 ± 0.18a 18.15 ± 0.26a 17.72 ± 0.15b 18.29 ± 0.47a 17.25 ± 0.26b 19.54 ± 0.26a 18.30 ± 0.18a 20.51 ± 0.25a 17.60 ± 0.19b 18.96 ± 0.27a 18.44 ± 0.21a
22.54 ± 0.26b 23.86 ± 0.32 23.88 ± 0.18a 27.28 ± 0.58a 23.48 ± 1.40b 21.47 ± 1.19a 21.72 ± 2.31b 23.31 ± 1.41a 22.78 ± 0.45b 23.87 ± 0.12a 22.74 ± 0.29b 23.14 ± 0.25a 22.47 ± 0.32b
28.45 ± 0.83b 27.89 ± 0.11 28.57 ± 0.25a 31.26 ± 0.26a 27.26 ± 1.06b 25.11 ± 1.24a 26.73 ± 2.34b 24.41 ± 1.29a 26.54 ± 0.58a 25.52 ± 0.33a 26.45 ± 0.22b 26.96 ± 0.21a 26.12 ± 0.12a
1.91 ± 0.70a 1.43 ± 0.25 0.36 ± 0.18b 0.02 ± 0.01b 0.04 ± 0.02b 0.00 ± 0.00b 0.01 ± 0.01b 0.00 ± 0.00b 0.38 ± 0.28b 0.00 ± 0.00b 0.00 ± 0.00b 0.07 ± 0.02b 0.00 ± 0.00b
55.56 66.67 22.22 13.04 5.56 0.00 2.70 0.00 28.57 0.00 0.00 20.00 0.00
Different letters at each column indicate significant difference (P < 0.05) after the multiple comparisons with Duncan method. Because size of sample collected in 1974 is too small (n = 6), the data are not compared to others.
137
dance distribution shifted northwards (between 31°00′–32°00′N and 122°50′–123°30′E) (Fig. 3). Surface and bottom temperatures in the areas (between 30°00′–32°00′N and 122°00′–123°30′E) where the greatest E. pacifica abundance occurred in the spring were 18.7– 20.6°C in 1959 and 18.1–20.7°C in 2002. ST and BT recorded in the spring of 2002 were significantly higher (Student’s t-test, ST: t52 = 7.18, P = 0.0001; BT: t52 = 6.00, P = 0.0001) than those recorded in 1959. Euphausia pacifica abundance of the spring of 2002 was significantly smaller than in 1959 (Student’s t-test, t52 = 2.16, P = 0.0393), specifically a dramatic decline in the spring of 2002 (Table 2). Comparison of distribution and abundance between the spring of
1959 and 2005 Distribution and abundance comparisons in the spring (from March to June) 1959 and 2005 are shown in Fig. 4. In 1959, the highest abundance was observed in May and June (Fig. 4). From March to May, Euphausia pacifica was broadly distributed in almost all of the study area, and E. pacifica shifted northward in June (Fig. 4). In May the highest abundance (10–20 ind.m–3) occurred in the southern area < 30°00′N. However, the area of highest abundance shifted to the north part (31°00′–32°00′N and 122°00′– 123°00′E) in June (Fig. 4). Temperature in the area (28°00′– 30°00′N and 122°00′–124°00′E) where the greatest abundance was observed in May 1959 was 2–3°C higher in June 1959 than in May 1959 (Table 3). Euphausia pacifica was not found in March, April, and June 2005, only was present in May 2005 in very low abundance (< 1.0 ind.m–3) (Fig. 4).
Fig. 2. Interannual sea surface temperature anomalies in May of 1971–2011. Data are recorded with satellite AVHRR (average temperature is 18.33°C).
to 2012 except 2010 (Fig. 2). Comparison of seasonal distribution and abundance between 1959 and 2002 Seasonal distribution patterns of Euphausia pacifica in 1959 and 2002 are shown in Fig. 3. In 1959, the highest abundance occurred in the spring (Fig. 3); in contrast, abundance was obviously smaller in the spring of 2002 than in 1959 (Fig. 3). In 1959, this was mainly distributed in both the north and south areas in the spring, and in the north area (between 30°00′–32°00′N and 122°00′–123°30′E) in the autumn (Fig. 4) where the surface and bottom temperatures in the spring were 15.9–17.8°C and 14.6–18.3°C, respectively. In the autumn of 2002, its region of the highest abun-
Interannual abundance change in spring Since 2002, abundance of Euphausia pacifica has decreased significantly (Duncan multiple test, P < 0.05) in May compared to that of 1959 (Table 1). Simultaneously the occurrences of the krill also dramatically declined since 2002 compared to 1959 (Table 1). Euphausia pacifica individuals have been recorded only in a few stations since 2004, and virtually disappeared entirely in 2005, 2007, 2009, 2010, and 2012 (Table 1). In 1974, E. pacifica was apparently still abundant (1.64 ind.m–3) (Table 1). Abundance and temperature The association between Euphausia pacifica abundance and surface/bottom temperatures in 1959 and 2002 is presented in Fig. 5. Data collected in both 1959 and 2002 indicate that the peak abundance of E. pacifica occurred at around 18°C (Fig. 5), although it was distributed in a wide range of temperatures (Fig. 5). Temperature range for E. pacifica abundance did not changed since 1959, with the greatest abundance observed at around 18°C (Fig. 5).
138
Fig. 3.
Z.-L. Xu and D. Zhang
Comparison of seasonal spatial distribution of Euphausia pacifica in the East China Sea in 1959 and 2002.
Fig. 4. Spatial distribution of Euphausia pacifica in the East China Sea in the spring (March–June) 1959 and in May 2005, no occurrence in March, April, and June 2005.
Declines in Euphausia pacifica abundance
139
Table 2. Comparison in surface temperature (ST), bottom temperature (BT), surface salinity (SS), bottom salinity (BS), abundance (A) and occurrence (O) between 1959 an 2002 (mean ± s.e., n = 27, Student’s t-test, df = 52). Season
Year
ST (°C)
BT (°C)
SS
BS
A (ind m–3)
O (%)
Spring
1959 2002 t P 1959 2002 t P 1959 2002 t P 1959 2002 t P
17.86 ± 0.21 19.53 ± 0.20 7.18 0.0001 26.80 ± 0.24 27.26 ± 0.11 1.74 0.0901 19.17 ± 0.33 18.84 ± 0.26 0.79 0.4322 9.18 ± 0.25 10.36 ± 0.33 2.84 0.0064
17.08 ± 0.32 19.58 ± 0.18 6 0.0001 22.76 ± 0.47 23.08 ± 0.52 0.46 0.6492 19.43 ± 0.32 20.06 ± 0.31 1.43 0.1589 9.60 ± 0.34 10.99 ± 0.37 2.76 0.0077
27.34 ± 0.98 29.33 ± 1.19 1.29 0.2043 29.03 ± 1.00 16.77 ± 1.07 8.37 0.0001 30.71 ± 0.81 15.97 ± 0.99 11.48 0.0001 28.49 ± 0.93 25.58 ± 1.35 1.77 0.0830
30.65 ± 1.02 31.66 ± 0.63 0.84 0.4045 31.41 ± 0.86 30.56 ± 0.85 0.70 0.4878 31.41 ± 0.73 30.16 ± 0.83 1.14 0.2613 30.21 ± 0.91 29.39 ± 1.35 0.50 0.6178
1.91 ± 0.70 0.36 ± 0.18 2.16 0.0393 0.06 ± 0.03 0.07 ± 0.04 0.33 0.7442 2.38 ± 0.80 1.69 ± 1.22 0.47 0.641 0.40 ± 0.10 0.09 ± 0.05 2.66 0.0111
55.56 22.22
Summer
Autumn
Winter
11.11 18.52
65.52 27.59
51.72 31.03
Table 3. Mean surface temperature (ST), bottom temperature (BT), surface salinity (SS), bottom salinity (BS), mean abundance (A) and maximum abundance (MA) of Euphausia pacifica in February– July, 1959 (mean ± s.e., n = 40). Month
ST (°C)
BT (°C)
SS
February March April May June July
8.02 ± 0.36 9.02 ± 0.17 12.29 ± 0.12 17.23 ± 0.14 20.32 ± 0.15 25.71 ± 0.19
8.57 ± 0.42 9.33 ± 0.25 12.65 ± 0.24 16.78 ± 0.20 19.05 ± 0.13 20.71 ± 0.24
29.76 ± 0.23 28.39 ± 0.19 27.86 ± 0.14 27.34 ± 0.13 28.37 ± 0.31 28.11 ± 0.17
BS 30.77 30.17 30.25 30.65 30.05 30.31
± 0.42 ± 0.26 ± 0.52 ± 0.57 ± 0.15 ± 0.28
MA (ind m–3)
A (ind m–3)
0.50 5.00 5.00 14.00 18.00 0.50
0.11 ± 0.03b 0.32 ± 0.12b 0.58 ± 0.13b 1.26 ± 0.40a 1.18 ± 0.48a 0.10 ± 0.03b
Different letters at each column indicate significant difference (P < 0.05) after the multiple comparisons with Duncan method.
Fig. 5. Relationship between sea surface and bottom temperatures and abundance of Euphausia pacifica in May 1959 (A, B) and 2002 (C, D) in the East China Sea.
DISCUSSION The results described here suggest an apparent relationship between Euphausia pacifica abundance and a regional warming probably associated to a general trend of global warming. A time series of ST and BT in the East China Sea showed that the ST and BT are clearly getting warmer. The trend of temperature variability was dominated by negative anomalies between 1960 and 1986, and has been greatly influenced by positive anomalies since 1987 to present at some areas in the East China Sea (Chen et al., 2005). Our data also show a rising trend of ST and BT in the East China Sea (Table 1), and positive temperature anomalies (1–2.5°C) from 1997 to 2012, except 2006 and 2010 (Fig. 2). Although abundance data of this study was not continuous, significant decline in abundance of E. pacifica in the East China Sea in recent years coincides with the temperature rising trend. In the spring of 1959 and 1974, the mean E. pacifica abundance reached 1.91 ind.m–3 and 1.64 ind.m–3, respectively (Table 1). However, this species nearly disappeared in the spring in the East China Sea since 2002 (Table 1). From the combined laboratory investigation and field data, 18°C may be the upper temperature limit for normal physiological process. Temperatures > 18°C result in shrinking between successive molts of E. pacifica (Marinovic and Mangel, 1999), decreasing brood sizes (Gómez-Gutiérrez et al., 2007) and egg hatching success, and high larval mortality (Iguchi and Ikeda, 1994). Dramatic reduction in E. pacifica abundance in the East China Sea since 2002 is probably a result of continuous stress from high temperature of > 19°C during the 1997–2002 period (Fig. 2, Wu et al., 2011). Euphausia pacifica abundance decline may also result
140
Z.-L. Xu and D. Zhang
from low productivity in the marine ecosystem (Richardson and Schoeman, 2004), as detected in zooplankton biomass from the southern California shores where increased ST resulted in increased stratification which was thought to restrict the nutrients supplied to the shallower layer by upwelling events (Roemmich and McGowan, 1995). However, the East China Sea, especially the Changjiang River estuary and adjacent waters, is one of the most productive waters in the world due to large quantities of nutrients delivered by the Changjiang River (Chen and Shen, 1999; Tu and Wang, 2006), and there is no evident seasonal stratification such as reported in southern California (Su and Yuan, 2005; Table 1). Therefore nutrients may not be a limiting factor to the primary productivity in this area. Temporal distribution shift and species turnover is another response of marine animals to climate change (e.g., Beaugrand et al., 2002; Perry et al., 2005; Greenstein and Pandolfi, 2008; Hillebrand et al., 2012). Distribution of Euphausia pacifica in the East China Sea was temperature related (Figs. 3 and 4). Generally, warm-water krill species become common in shelf waters in response to the warm temperatures positive anomaly, and some temperate krill species return to their previous habitat when temperature becomes normal (see review by Walther et al., 2002), as shown by some euphausiid species in Baja California waters (Gómez-Gutiérrez et al., 1995). Abundance of a warm-water species in China, Pseudeuphausia sinica, has increased abundance since 1963 in the East China Sea (Ning and Jiang, 1991; Xu, 2007; Gao and Xu, 2011). The abundance of P. sinica increased from 0.18–0.21 ind.m–3 in 1979 and 1981 to 0.68–4.00 ind./m3 in the period of 2000–2007 (Gao and Xu, 2011). Abundant warm-water krill species (Ning and Jiang, 1991; Xu, 2007; Gao and Xu, 2011) and other zooplankton, such as a dominated copepod Calanus sinicus with the same spatial and termporal distribution, (Chen et al., 2011) in the East China Sea suggests that pollution is not a factor causing E. pacifica population decline in the region. Seasonal distribution of Euphausia pacifica in the East China Sea reflects the fact that its distribution was probably temperature related (Fig. 3) as in the Yellow Sea (Yoon et al., 2000; Sun et al., 2011). The greatest abundance of E. pacifica has occurred in the spring and autumn, and E. pacifica almost disappeared in the summer (Fig. 3), implying that E. pacifica probably migrated deeper or drifted northward with regional circulation when high temperature occurs in the summer, and returned to the previous distribution areas with the Yellow Sea Coastal Current when the temperature had fallen to the 1959 range in the autumn (Fig. 6). Both inter-annual (between November 1959 and 2002) (Fig. 3) and inter-monthly (between May and June, 1959) (Fig. 4) comparisons suggest that E. pacifica has had a circulation-driven northward movement in the East China Sea since 1959. Historic data has shown that E. pacifica were observed in the Taiwan strait (Hansen, 1915; Cai, 1978), and southward to north part of the South China Sea (Chen and Zhang, 1983). However, there were no observations of E. pacifica in the waters < 28°N in 1998 (Xu, 2007; present study). It has been suggested that assemblages of Euphausia pacifica in the Yellow Sea and East China Sea correlate geographically with the positions of the water masses and
Fig. 6. Water circulation patterns in the East China Sea. CCC: East China Sea Coastal Current; CDW: Changjiang dilute water; TC: Tsushima Current; TWC: Taiwan Current; YSCC: Yellow Sea Cold Current; YSWC: Yellow Sea Warm Current.
currents (Cai, 1986; Wang et al., 2003; Sun et al., 2011). Current study supports the speculation (see above). The connection between the Yellow Sea and East China Sea is primarily through the Yellow Sea Coastal Current and the Taiwan Warm Current (Fig. 6). In addition, the E. pacifica living in the south part (the area south of 34°N) of the Yellow Sea and East China Sea are the same genetically populations (Guo, 2002), suggesting that there is connection between the East China Sea and Yellow Sea populations. Although E. pacifica is currently still abundant in the Yellow Sea (Liu, 2002; Sun et al., 2011; Liu et al., 2012), the question arises: why does E. pacifca in the Yellow Sea not return to the East China Sea when temperature in the East China Sea declined with the Yellow Sea Coast Current? For example, both ST and BT in 2004 and 2006 were relatively similar to that recorded in 1959, but abundance level of the E. pacifica was 0.01 ind.m–3 in May 2006 compared to 1.91 ind.m–3 in May 1959 (Table 1). Further study on the connections between the two populations is essential to reveal the reasons why the E. pacifica population in the East China Sea has not recovered. It is well known that many zooplankton species have geographical distributions that correlate to water masses and circulation patterns (Brinton, 1962). It has been suggested that the distribution of E. pacifica in the East China Sea is related to the cold water mass from the Yellow Sea Current (Wang et al., 2003). However, no direct evidence supports a relationship between the distribution of E. pacifica and the cold water mass in the East China Sea because
Declines in Euphausia pacifica abundance
temperatures in the most abundant areas were not different from those with low abundance levels (Fig. 5). The seasonal distribution (low abundance or disappearance in summer) of E. pacifica (Fig. 3) also reflects that there is no cold water mass in the East China Sea in summer (Su and Yuan, 2005). Therefore, the present data collected in 1959 suggest that E. pacifica was probably advected from the survey areas in summer not being present in water masses with high temperature. Furthermore, we could hypothesize that temperature in the area where E. pacifica (the East China Sea population) inhabit during summer may be anomalous due to the regional warming as well, resulting in the disappearance of the population. Data presented in this study indicate that temporal variability of biological processes and identification of the main factors that drive the dynamic change of marine ecosystems may be complex. We believe the decline of E. pacifica abundance in the East China Sea is a regional response to global warming, but to understand the overall impact, additional factors affecting the E. pacifica distribution and abundance need to be investigated in future studies as have been done in the California Current System by the CalCOFI (1957 to present) and IMECOCAL (1997 to present) research programs. ACKNOWLEDGMENTS This study was funded by the National Science Foundation of China (No. 41176131) and the National Key Program for Fundamental Research and Development (Project 973) (No. 2010CB428705).
REFERENCES Beaugrand G, Reid PC (2003) Long-term changes in phytoplankton, zooplankton and salmon related to climate. Glob Change Biol 9: 801–817 Beaugrand G, Reid PC, Ibañez F, Lindley JA, Edwards M (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296: 1692–11694 Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466: 591–596 Brinton E (1962) The distribution of Pacific euphausiids. Bull Scripps Inst Oceanogr 8: 51–270 Brinton E, Townsend AW (2003) Decadal variability in abundances of the dominant euphausiid species in Southern Sectors of the California Current. Deep-Sea Res II 50: 2449–2472 Cai BJ (1978) Taxonomy study on the Euphausiacea (Crustacea) from the South Yellow Sea and East China Sea. Ocean Sci Tech 8: 39–56 Cai BJ (1986) Distribution of the Euphausiids in the Yellow Sea and the East China Sea. Study collection of crustaceans. Science Press, Beijing, pp 140–146 Chen Q-C, Zhang G-X (1983) Study on Euphausiacea in the central and northern parts of the South China Sea. In “Collected Papers on marine biology in the South China Sea” Ed by Morton B, Hong Kong University Press, Beijing, pp 139–171 Chen Y-Q, Shen X-Q (1999) Changes in the Biomass of the East China Sea Ecosystem. In “Large marine ecosystems of the Pacific rim-assessment, sustainability, and management” Ed by Sherman K, Tang Q-S, Blackwell Science, Malden, pp 221–239 Chen M-R, Shi S-H, Shen H-M (2005) The relationship between sea surface temperature and El Niño events. Mar Forec 22: 80–85 Chen H-J, Qi Y-P, Liu G-X (2011) Spatial and temporal variations of macro- and mesozooplankton community in the Huanghai Sea (Yellow Sea) and East China Sea in summer and winter. Acta
141
Oceanol Sin 30: 84–95 Chiba S, Tadokoro K, Sugisak H, Saino T (2006) Effects of decadal climate change on zooplankton over the last 50 years in the western subarctic North Pacific. Glob Change Biol 12: 907–920 Dippner J, Hänninen J, Kuosa H, Vuorinen I (2001) The influence of climatic variability on zooplankton abundance in the Northern Baltic Archipelago Sea (SW Finland). ICES J Mar Sci 58: 569– 578 Falkowski PG, Barber RT, Smetacekv V (1998) Biogeochemical Controls and Feedbacks on Ocean Primary Production. Science 281: 200–206 Gao Q, Xu Z-L (2011) Effect of regional warming on the abundance of Pseudeuphausia sinica Wang et Chen (Euphausiacea) off the Changjiang River (Yangtze River) estuary. Acta Oceanol Sin 30: 122–128 Gómez-Gutiérrez J, Palomares-García R, Gendron D (1995) Community structure of the euphausiid populations along the west coast of Baja California, Mexico, during the weak ENSO 1986– 1987. Mar Ecol Prog Ser 120: 41–51 Gómez-Gutiérrez J, Feinberg LR, Shaw T, Peterson WT (2007) Interannual and geographical variability of the brood size of the euphausiids Euphausia pacifica and Thysanoessa spinifera along the Oregon coast (1999–2004). Deep Sea Res I 54: 2145–2169 Greenstein BJ, Pandolfi JM (2008) Escaping the heat: range of reef coral taxa in costal Western Australia. Glob Change Biol 14: 513–528 Guo D-H (2002) Molecular ecology studies on genetic diversity and differentiation of common krill in China seas. Ph.D. Thesis, Xiamen University Hansen HJ (1915) The Crustacea Euphausiacea of the United States Museum. Proc U.S. Natl Mus 48: 59–114 Hillebrand H, Burgmer T, Biermann E (2012) Running to stand still: temperature effects on species richness, species turnover, and functional community dynamics. Mar Biol 159: 2415–2422 Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15: 56–61 Iguchi N, Ikeda T (1994) Experimental study on brood size, egg hatchability and early development of a Euphasuiil Euphausia pacifica from Toyama Bay, Southern Japan Sea. Jpn Sea Natl Fish Res Inst 44: 49–57 Lavaniegos BE, Ohman MD (2007) Coherence of long-term variations of zooplankton in two sectors of the California Current System. Prog Oceanogr 75: 42–69 Linacre L (2004) Community structure of Euphausiids in the Southern part of the California current during October 1997 (El Niño) and October 1999 (La Niña). CalCOFI Rep 45: 126–135 Liu H-L (2002) Ecological study on the Yellow Sea and the East China Sea. Ph.D. Thesis. Oceanic Institution, Qingdao Liu P, Song H-J, Wang X, Wang Z-L, Pu X-M, Zhu M-Y (2012) Seasonal variability of the zooplankton community in the southwest of the Huanghai Sea (Yellow Sea) Cold Water Mass. Acta Oceanol Sin 31: 127–139 Mackas DL, Thomson RE, Galbraith M (2001) Changes in the zooplankton community of the British Columbia continental margin, 1985–1999, and their covariation with oceanographic conditions. Can J Fish Aquatic Sci 58: 685–702 Marinovic B, Mangel M (1999) Krill can shrink as an ecological adaptation to temporally unfavorable conditions. Ecol Lett 2: 338–243 Molinero JK, Ibanez F, Souissi S, Buecher E, Dallot S, Nival P (2008) Climate control on the long-term anomalous changes of zooplankton communities in the Northwestern Mediterranean. Glob Change Biol 14: 11–26 Nemoto T (1957) Foods of baleen whales in the northern Pacific. Sci Rep Whales Res Inst 12: 33–90 Ning X-R, Jiang J-X (1991) Marine atlas of Bohai Sea, Yellow Sea
142
Z.-L. Xu and D. Zhang
and East China Sea: Biology. China Ocean Press, Beijing (in Chinese) Ogi H, Tanaka H (1984) Distribution and feeding of the typical sea birds in the subarctic zone of the North Pacific. Gekkan Kaiyo 16: 205–211 Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42 Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308: 1912–1915 Rebstock G (2002) Climatic regime shifts and decadal-scale variability in calanoid copepod populations off southern California. Glob Change Biol 8: 71–89 Richardson AJ, Schoeman DJ (2004) Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305: 1609–1612 Roemmich D, McGowan J (1995) Climate warming and the decline of zooplankton in the California current. Science 267: 1324–1325 Su J-N, Yuan Y-L (2005) Hydrology of China coastal waters. China Ocean Press, Beijing (in Chinese) Sun S, Tao Z-C, Li C-L, Liu H-L (2011) Spatial distribution and population structure of Euphausia pacifica in the Yellow Sea (2006–2007). J Plankton Res 33: 873–889 Tanasichuk RW (1998) Interannual variation in the population biology and productivity of Euphausia pacifica in Barkely Sound, Canada, with special reference to the 1992 and 1993 warm ocean years. Mar Ecol Prog Ser 173: 163–180 Tanasichuk RW, Ware DM, Shaw W, McFarlane GA (1991) Varia-
tion in the diet, daily ration and feeding periodicity of Pacific hake (Merluccius productus) and spiny dogfish (Squalus acanthias) off the lower west coast of Vancouver Island. Can J Fish Aquatic Sci 48: 2118–2128 Tu J-B, Wang B-D (2006) Assessment of eutrophication status in the Changjiang River estuary and its adjacent waters. Adv Mar Sci 24: 532–538 Walther G, Post E, Convey P, Menzel A, Parmesanll C, Beebee TJC, et al. (2002) Ecological responses to recent climate change. Nature 416: 389–395 Wang R, Chen Y-Q, Zuo T, Wang K (2003) Quantitative distribution of euphausiieds in the Yellow Sea and the East China Sea in spring and autumn in relation to the hydrographic conditions. J Fish Chn 27 (suppl.): 31–38 Wu Y-M, Xu Z-L, Fan W, Chui X-S (2011) Change of sea surface temperature in the East Chian Sea during 1985–2005. Acta Oceanol Sin 33: 9–18 Xu Z-L (2007) Distribution patterns of pelagic euphausiids in the East China Sea. Acta Ecol Sin 27: 1–9 Yamamura O, Inada T, Shimazaki K (1998) Predation on Euphausia pacifica by demersal fshes: predation impact and influence of physical variability. Mar Biol 132: 185–208 Yoon WD, Cho SH, Lim D, Choi YK, Lee Y (2000) Spatial distribution of Euphausia pacifica (Euphausiacea: Crustacea) in the Yellow Sea. J Plankton Res 22: 939–949 (Received August 2, 2013 / Accepted November 15, 2013)
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
¤ 2014 Zoological Society of Japan
ZOOLOGICAL SCIENCE 31: 135–142 (2014)
Dramatic Declines in Euphausia pacifica Abundance in the East China Sea: Response to Recent Regional Climate Change Zhao-Li Xu and Dong Zhang* East China Sea Fisheries Research Institute, Chinese Academy of Fisheries Science, Jun Gong Road, Shanghai 200090, China
As with other marine ecosystems around the world, water temperature has been anomalously warm in recent years in the East China Sea. We analyzed historical data to explore the effects of climatic change on the abundance and distribution variation of Euphausia pacifica in the East China Sea (the Changjiang River estuary and adjacent areas). In 1959, the highest abundance occurred in the spring and autumn, and this krill species was still abundant in May 1974; however, its abundance was significantly reduced in 2002, markedly in spring. Euphausia pacifica was the numerically dominant euphausiid in the East China Sea in 1959. Its mean abundance was up to 1.91 ind m–3 and 1.64 ind/m3 in 1959 and 1974, respectively; however, this figure decreased to 0.36 ind m–3 in 2002. Since 2003, the abundances have been near zero in the most years. Both inter-annual (between November 1959 and 2002) and inter-monthly (between May and June 1959) comparisons suggest that E. pacifica has had a temperature-driven northward movement in response to rising sea surface temperature, especially the positive anomalies since 1997. However, E. pacifica did not come back to the previous habitat when temperature became relative cold. Hence additional factors affecting the E. pacifica distribution and abundance need to be investigated in the future study. Key words: Euphausia pacifica, global warming, abundance, distribution shift, East China Sea, temperature anomaly INTRODUCTION The effects of climate change on species and communities can be examined through physiological changes, distributions, phenology, and regional adaptations (Hughes, 2000). Modification of the distribution range of pelagic organisms is a sensitive and well-documented indicator of climate change (e.g., Beaugrand et al., 2002; Perry et al., 2005; Greenstein and Pandolfi, 2008). How global climate change might affect phytoplankton is a marked concern because they play a fundamental role in the food web by providing half the global primary production (Falkowski et al., 1998; Boyce et al., 2010). Many studies have explored the impact of climatic change on zooplankton biomass and community structure across distinct geographic regions, such as California coastal waters (Roemmich and McGowan, 1995; Rebstock, 2002; Brinton and Townsand, 2003), the Northern Baltic Archipelago Sea (Dippner et al., 2001), North Atlantic (Beaugrand et al., 2002; Beaugrand and Reid, 2003), Northeast Atlantic (Richardson and Schoeman, 2004), subarctic North Pacific (Chiba et al., 2006), and the Northwestern Mediterranean Sea (Molinero et al., 2008). Responses of zooplankton to temperature variability vary regionally depending on community structure and local oceanographic conditions. For example, the krill-like Euphausia pacifica shrinks (Marinovic and Mangel, 1999) * Corresponding author. Tel. : +86-21-65684655; Fax : +86-21-65683926; E-mail : [email protected] doi:10.2108/zsj.31.135
and decrease its brood sizes (Gómez-Gutiérrez et al., 2007) and egg hatch success (Iguchi and Ikeda, 1994) in response to elevated water temperatures. Distribution shift and species composition change are likely the most immediate responses to regional climate change in the pelagic ecosystem (Tanasichuk, 1998; Mackas et al., 2001; Beaugrand et al., 2002). Compared with the extensive zooplankton sampling effort in California Current System, we do not understand how climate change impacts on the marine ecosystem of the Western Pacific, especially off the Chinese coastal waters, due to comparatively limited information to date obtained. In the present study, we investigated the interannual temperature impact on the krill species E. pacifica in the East China Sea (the Changjiang River estuary and adjacent area). The East China Sea is greatly influenced by the runoff from the Changjiang River, the Yellow Sea Coastal Current and the Taiwan Current (Su and Yuan, 2005). There is no evident stratification season in the East China Sea, especially in the area studied (Su and Yuan, 2005). This area is one of the most productive waters in the world due to nutrient runoffs from the Changjiang River and provides spawning and nursery grounds for numerous species of pelagic fish species (Chen and Shen, 1999; Tu and Wang, 2006). Understanding the effect of global climate change on plankton communities is essential to regulate the fisheries’ resource exploitation and management from this region of China. Euphausia pacifica is the dominant euphausiid species in the East China Sea, being the only Euphausia species with temperate zoogeographic distribution in the North Pacific (Brinton, 1962). It is considered one of the key zoo-
136
Z.-L. Xu and D. Zhang
plankton species in the food web of the northwestern Pacific, serving as prey for many endemic and migrant fish species, marine mammals, and sea birds (Nemoto, 1957; Ogi and Tanaka, 1984; Tanasichuk et al., 1991; Yamamura et al., 1998). Euphausia pacifica is mainly distributed in the Yellow Sea in China (Cai, 1986). In the East China Sea, E. pacifica is mainly distributed in the Changjiang estuary and adjacent areas (29–32°N, 121.5–123.5°E), with high abundance in the spring and autumn (Xu, 2007). The spatial and temporal distribution of E. pacifica in the Yellow Sea and East China Sea is significantly affected by the Yellow Sea Bottom Cold Water (YSBCW) which offers the species a refuge from warm surface water in summer and autumn (Cai, 1986; Sun et al., 2011), The spatial distribution of the species is primarily controlled by seawater temperature (Yoon et al., 2000; Sun et al., 2011). Thus this species may also be a sensitive indicator of regional sea warming, as several reports have shown significant abundance changes of E. pacifica off the coast of California and Baja California after the 1976 climate regime (Gómez-Gutiérrez et al., 1995; Linacre, 2004; Lavaniegos and Ohman, 2007). We studied E. pacifica to examine the effects of climate change occurred between 1959 and 2012 in the East China Sea. We analyzed historical data to explore the effects of temperature increase on abundance and distribution patterns of E. pacifica in the Changjiang estuary and adjacent areas. MATERIALS AND METHODS
bottom salinity (SS and BS) were recorded at each sampling site with an SBE-19 CTD, except in 1959 and 1974 when surface and seafloor temperature was measured with a simplified reversing thermometer, and salinity was determined with hydrometer. Bottom depths of the sampling sites were 40–200 m, but mostly collected at 50–100 m depth. To show temperature trend, sea surface temperatures recorded in May of 1971–2011 with the satellite AVHRR in area between 28°30′–32°00′N and 121°30′–123°30′E were obtained. This allows us to study long-term anomalous temperature change. Data analysis We made a comparison of Euphausia pacifica abundance (ind.m–3) and distribution change using data collected in 1959 and 2002–2012. Seasonal comparisons were done using data from 1959 and 2002. Data from spring of 1959 and 2002, and 1959 and 2005 were also compared. Euphausia pacifica relative occurrence is shown as the percentage of stations where this species was present over the entire region. Mean values of abundances and temperatures were initially tested for normality and homogeneity of variance and then Duncan multiple comparisons was applied to test significance of interannual difference in mean E. pacifica abundances and temperatures. Statistical analyses were performed using SPSS 11.5.
RESULTS Interannual variation of temperature in spring In the East China Sea, ST and BT in May of recent years (except ST in 2004, 2006, 2008, and 2010, and BT in 2004, 2006, and 2010 years), were significantly higher (Duncan multiple test, P < 0.05) than those in 1959 (Table 1). Sea surface temperature (satellite data) in the East China Sea was generally below average before 1997 (temperatures in only four of 26 years were above average, 18.33°C), followed by a marked upward pattern from 1997
Study area and sampling To assess the abundance and distribution of Euphausia pacifica, we collected zooplankton samples between 29°00′–32°00′N and 122°00′–123°30′E (Fig. 1). In 1959, data were obtained from collections made in the winter (February), spring (from March to June), summer (August), and autumn (November). In 2002, data were collected in the winter (February), spring (May), summer (August), and autumn (November). From 2003 to 2012, the surveys were conducted only in the spring (May). Three additional surveys were conducted in March, April, and June of 2005. Moreover, data collected at six stations in the area in May 1974 were also presented, as supplemental evidence. Euphausiids were sampled during the day in all years by towing a zooplankton net with an 80-cm diameter mouth and 505-μm mesh vertically from near the bottom to the surface. The volume of water filtered was measured with a flow meter mounted at the net mouth. Abundance (ind.m–3) was estimated from water volume filtered and the mean for all sampling stations was calculated. For comparison purposes data collected at the same stations for each year over the years were used to estimate mean E. pacifica abundance. For example 27 sampling stations were selected to compare mean abundance between 1959 and the 2002–2012 period, and 40 sampling stations to compare mean abundance in February–June of 1959 (Fig. 1). The samples were immediately preserved in 5% formalin buffered with Sodium Fig. 1. Map of sampling stations. (A) sampling stations both in 1959 and 2002–2012, and borate. Surface (ST) and bottom (BT) temsix sampling stations in 1974; (B) sampling stations in 1959 (see Materials and Methods for perature (5 m from bottom), and surface and details).
Declines in Euphausia pacifica abundance Table 1. Surface temperature (ST), bottom temperature (BT), surface salinity (SS), bottom salinity (BS), abundance (A), and occurrence (O) in May 1959, 1974 and 2002–2012 (mean ± s.e., n = 27). Year
ST (°C)
BT (°C)
SS
BS
A (ind.m–3)
O (%)
1959 1974 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
17.86 ± 0.21b 17.40 ± 0.22 19.53 ± 0.20a 18.95 ± 0.23a 18.34 ± 0.21b 18.94 ± 0.30a 18.51 ± 0.35b 19.94 ± 0.27a 18.63 ± 0.16b 20.90 ± 0.29a 17.84 ± 0.29b 19.03 ± 0.25a 18.67 ± 0.22b
17.08 ± 0.32b 17.12 ± 0.21 19.58 ± 0.18a 18.15 ± 0.26a 17.72 ± 0.15b 18.29 ± 0.47a 17.25 ± 0.26b 19.54 ± 0.26a 18.30 ± 0.18a 20.51 ± 0.25a 17.60 ± 0.19b 18.96 ± 0.27a 18.44 ± 0.21a
22.54 ± 0.26b 23.86 ± 0.32 23.88 ± 0.18a 27.28 ± 0.58a 23.48 ± 1.40b 21.47 ± 1.19a 21.72 ± 2.31b 23.31 ± 1.41a 22.78 ± 0.45b 23.87 ± 0.12a 22.74 ± 0.29b 23.14 ± 0.25a 22.47 ± 0.32b
28.45 ± 0.83b 27.89 ± 0.11 28.57 ± 0.25a 31.26 ± 0.26a 27.26 ± 1.06b 25.11 ± 1.24a 26.73 ± 2.34b 24.41 ± 1.29a 26.54 ± 0.58a 25.52 ± 0.33a 26.45 ± 0.22b 26.96 ± 0.21a 26.12 ± 0.12a
1.91 ± 0.70a 1.43 ± 0.25 0.36 ± 0.18b 0.02 ± 0.01b 0.04 ± 0.02b 0.00 ± 0.00b 0.01 ± 0.01b 0.00 ± 0.00b 0.38 ± 0.28b 0.00 ± 0.00b 0.00 ± 0.00b 0.07 ± 0.02b 0.00 ± 0.00b
55.56 66.67 22.22 13.04 5.56 0.00 2.70 0.00 28.57 0.00 0.00 20.00 0.00
Different letters at each column indicate significant difference (P < 0.05) after the multiple comparisons with Duncan method. Because size of sample collected in 1974 is too small (n = 6), the data are not compared to others.
137
dance distribution shifted northwards (between 31°00′–32°00′N and 122°50′–123°30′E) (Fig. 3). Surface and bottom temperatures in the areas (between 30°00′–32°00′N and 122°00′–123°30′E) where the greatest E. pacifica abundance occurred in the spring were 18.7– 20.6°C in 1959 and 18.1–20.7°C in 2002. ST and BT recorded in the spring of 2002 were significantly higher (Student’s t-test, ST: t52 = 7.18, P = 0.0001; BT: t52 = 6.00, P = 0.0001) than those recorded in 1959. Euphausia pacifica abundance of the spring of 2002 was significantly smaller than in 1959 (Student’s t-test, t52 = 2.16, P = 0.0393), specifically a dramatic decline in the spring of 2002 (Table 2). Comparison of distribution and abundance between the spring of
1959 and 2005 Distribution and abundance comparisons in the spring (from March to June) 1959 and 2005 are shown in Fig. 4. In 1959, the highest abundance was observed in May and June (Fig. 4). From March to May, Euphausia pacifica was broadly distributed in almost all of the study area, and E. pacifica shifted northward in June (Fig. 4). In May the highest abundance (10–20 ind.m–3) occurred in the southern area < 30°00′N. However, the area of highest abundance shifted to the north part (31°00′–32°00′N and 122°00′– 123°00′E) in June (Fig. 4). Temperature in the area (28°00′– 30°00′N and 122°00′–124°00′E) where the greatest abundance was observed in May 1959 was 2–3°C higher in June 1959 than in May 1959 (Table 3). Euphausia pacifica was not found in March, April, and June 2005, only was present in May 2005 in very low abundance (< 1.0 ind.m–3) (Fig. 4).
Fig. 2. Interannual sea surface temperature anomalies in May of 1971–2011. Data are recorded with satellite AVHRR (average temperature is 18.33°C).
to 2012 except 2010 (Fig. 2). Comparison of seasonal distribution and abundance between 1959 and 2002 Seasonal distribution patterns of Euphausia pacifica in 1959 and 2002 are shown in Fig. 3. In 1959, the highest abundance occurred in the spring (Fig. 3); in contrast, abundance was obviously smaller in the spring of 2002 than in 1959 (Fig. 3). In 1959, this was mainly distributed in both the north and south areas in the spring, and in the north area (between 30°00′–32°00′N and 122°00′–123°30′E) in the autumn (Fig. 4) where the surface and bottom temperatures in the spring were 15.9–17.8°C and 14.6–18.3°C, respectively. In the autumn of 2002, its region of the highest abun-
Interannual abundance change in spring Since 2002, abundance of Euphausia pacifica has decreased significantly (Duncan multiple test, P < 0.05) in May compared to that of 1959 (Table 1). Simultaneously the occurrences of the krill also dramatically declined since 2002 compared to 1959 (Table 1). Euphausia pacifica individuals have been recorded only in a few stations since 2004, and virtually disappeared entirely in 2005, 2007, 2009, 2010, and 2012 (Table 1). In 1974, E. pacifica was apparently still abundant (1.64 ind.m–3) (Table 1). Abundance and temperature The association between Euphausia pacifica abundance and surface/bottom temperatures in 1959 and 2002 is presented in Fig. 5. Data collected in both 1959 and 2002 indicate that the peak abundance of E. pacifica occurred at around 18°C (Fig. 5), although it was distributed in a wide range of temperatures (Fig. 5). Temperature range for E. pacifica abundance did not changed since 1959, with the greatest abundance observed at around 18°C (Fig. 5).
138
Fig. 3.
Z.-L. Xu and D. Zhang
Comparison of seasonal spatial distribution of Euphausia pacifica in the East China Sea in 1959 and 2002.
Fig. 4. Spatial distribution of Euphausia pacifica in the East China Sea in the spring (March–June) 1959 and in May 2005, no occurrence in March, April, and June 2005.
Declines in Euphausia pacifica abundance
139
Table 2. Comparison in surface temperature (ST), bottom temperature (BT), surface salinity (SS), bottom salinity (BS), abundance (A) and occurrence (O) between 1959 an 2002 (mean ± s.e., n = 27, Student’s t-test, df = 52). Season
Year
ST (°C)
BT (°C)
SS
BS
A (ind m–3)
O (%)
Spring
1959 2002 t P 1959 2002 t P 1959 2002 t P 1959 2002 t P
17.86 ± 0.21 19.53 ± 0.20 7.18 0.0001 26.80 ± 0.24 27.26 ± 0.11 1.74 0.0901 19.17 ± 0.33 18.84 ± 0.26 0.79 0.4322 9.18 ± 0.25 10.36 ± 0.33 2.84 0.0064
17.08 ± 0.32 19.58 ± 0.18 6 0.0001 22.76 ± 0.47 23.08 ± 0.52 0.46 0.6492 19.43 ± 0.32 20.06 ± 0.31 1.43 0.1589 9.60 ± 0.34 10.99 ± 0.37 2.76 0.0077
27.34 ± 0.98 29.33 ± 1.19 1.29 0.2043 29.03 ± 1.00 16.77 ± 1.07 8.37 0.0001 30.71 ± 0.81 15.97 ± 0.99 11.48 0.0001 28.49 ± 0.93 25.58 ± 1.35 1.77 0.0830
30.65 ± 1.02 31.66 ± 0.63 0.84 0.4045 31.41 ± 0.86 30.56 ± 0.85 0.70 0.4878 31.41 ± 0.73 30.16 ± 0.83 1.14 0.2613 30.21 ± 0.91 29.39 ± 1.35 0.50 0.6178
1.91 ± 0.70 0.36 ± 0.18 2.16 0.0393 0.06 ± 0.03 0.07 ± 0.04 0.33 0.7442 2.38 ± 0.80 1.69 ± 1.22 0.47 0.641 0.40 ± 0.10 0.09 ± 0.05 2.66 0.0111
55.56 22.22
Summer
Autumn
Winter
11.11 18.52
65.52 27.59
51.72 31.03
Table 3. Mean surface temperature (ST), bottom temperature (BT), surface salinity (SS), bottom salinity (BS), mean abundance (A) and maximum abundance (MA) of Euphausia pacifica in February– July, 1959 (mean ± s.e., n = 40). Month
ST (°C)
BT (°C)
SS
February March April May June July
8.02 ± 0.36 9.02 ± 0.17 12.29 ± 0.12 17.23 ± 0.14 20.32 ± 0.15 25.71 ± 0.19
8.57 ± 0.42 9.33 ± 0.25 12.65 ± 0.24 16.78 ± 0.20 19.05 ± 0.13 20.71 ± 0.24
29.76 ± 0.23 28.39 ± 0.19 27.86 ± 0.14 27.34 ± 0.13 28.37 ± 0.31 28.11 ± 0.17
BS 30.77 30.17 30.25 30.65 30.05 30.31
± 0.42 ± 0.26 ± 0.52 ± 0.57 ± 0.15 ± 0.28
MA (ind m–3)
A (ind m–3)
0.50 5.00 5.00 14.00 18.00 0.50
0.11 ± 0.03b 0.32 ± 0.12b 0.58 ± 0.13b 1.26 ± 0.40a 1.18 ± 0.48a 0.10 ± 0.03b
Different letters at each column indicate significant difference (P < 0.05) after the multiple comparisons with Duncan method.
Fig. 5. Relationship between sea surface and bottom temperatures and abundance of Euphausia pacifica in May 1959 (A, B) and 2002 (C, D) in the East China Sea.
DISCUSSION The results described here suggest an apparent relationship between Euphausia pacifica abundance and a regional warming probably associated to a general trend of global warming. A time series of ST and BT in the East China Sea showed that the ST and BT are clearly getting warmer. The trend of temperature variability was dominated by negative anomalies between 1960 and 1986, and has been greatly influenced by positive anomalies since 1987 to present at some areas in the East China Sea (Chen et al., 2005). Our data also show a rising trend of ST and BT in the East China Sea (Table 1), and positive temperature anomalies (1–2.5°C) from 1997 to 2012, except 2006 and 2010 (Fig. 2). Although abundance data of this study was not continuous, significant decline in abundance of E. pacifica in the East China Sea in recent years coincides with the temperature rising trend. In the spring of 1959 and 1974, the mean E. pacifica abundance reached 1.91 ind.m–3 and 1.64 ind.m–3, respectively (Table 1). However, this species nearly disappeared in the spring in the East China Sea since 2002 (Table 1). From the combined laboratory investigation and field data, 18°C may be the upper temperature limit for normal physiological process. Temperatures > 18°C result in shrinking between successive molts of E. pacifica (Marinovic and Mangel, 1999), decreasing brood sizes (Gómez-Gutiérrez et al., 2007) and egg hatching success, and high larval mortality (Iguchi and Ikeda, 1994). Dramatic reduction in E. pacifica abundance in the East China Sea since 2002 is probably a result of continuous stress from high temperature of > 19°C during the 1997–2002 period (Fig. 2, Wu et al., 2011). Euphausia pacifica abundance decline may also result
140
Z.-L. Xu and D. Zhang
from low productivity in the marine ecosystem (Richardson and Schoeman, 2004), as detected in zooplankton biomass from the southern California shores where increased ST resulted in increased stratification which was thought to restrict the nutrients supplied to the shallower layer by upwelling events (Roemmich and McGowan, 1995). However, the East China Sea, especially the Changjiang River estuary and adjacent waters, is one of the most productive waters in the world due to large quantities of nutrients delivered by the Changjiang River (Chen and Shen, 1999; Tu and Wang, 2006), and there is no evident seasonal stratification such as reported in southern California (Su and Yuan, 2005; Table 1). Therefore nutrients may not be a limiting factor to the primary productivity in this area. Temporal distribution shift and species turnover is another response of marine animals to climate change (e.g., Beaugrand et al., 2002; Perry et al., 2005; Greenstein and Pandolfi, 2008; Hillebrand et al., 2012). Distribution of Euphausia pacifica in the East China Sea was temperature related (Figs. 3 and 4). Generally, warm-water krill species become common in shelf waters in response to the warm temperatures positive anomaly, and some temperate krill species return to their previous habitat when temperature becomes normal (see review by Walther et al., 2002), as shown by some euphausiid species in Baja California waters (Gómez-Gutiérrez et al., 1995). Abundance of a warm-water species in China, Pseudeuphausia sinica, has increased abundance since 1963 in the East China Sea (Ning and Jiang, 1991; Xu, 2007; Gao and Xu, 2011). The abundance of P. sinica increased from 0.18–0.21 ind.m–3 in 1979 and 1981 to 0.68–4.00 ind./m3 in the period of 2000–2007 (Gao and Xu, 2011). Abundant warm-water krill species (Ning and Jiang, 1991; Xu, 2007; Gao and Xu, 2011) and other zooplankton, such as a dominated copepod Calanus sinicus with the same spatial and termporal distribution, (Chen et al., 2011) in the East China Sea suggests that pollution is not a factor causing E. pacifica population decline in the region. Seasonal distribution of Euphausia pacifica in the East China Sea reflects the fact that its distribution was probably temperature related (Fig. 3) as in the Yellow Sea (Yoon et al., 2000; Sun et al., 2011). The greatest abundance of E. pacifica has occurred in the spring and autumn, and E. pacifica almost disappeared in the summer (Fig. 3), implying that E. pacifica probably migrated deeper or drifted northward with regional circulation when high temperature occurs in the summer, and returned to the previous distribution areas with the Yellow Sea Coastal Current when the temperature had fallen to the 1959 range in the autumn (Fig. 6). Both inter-annual (between November 1959 and 2002) (Fig. 3) and inter-monthly (between May and June, 1959) (Fig. 4) comparisons suggest that E. pacifica has had a circulation-driven northward movement in the East China Sea since 1959. Historic data has shown that E. pacifica were observed in the Taiwan strait (Hansen, 1915; Cai, 1978), and southward to north part of the South China Sea (Chen and Zhang, 1983). However, there were no observations of E. pacifica in the waters < 28°N in 1998 (Xu, 2007; present study). It has been suggested that assemblages of Euphausia pacifica in the Yellow Sea and East China Sea correlate geographically with the positions of the water masses and
Fig. 6. Water circulation patterns in the East China Sea. CCC: East China Sea Coastal Current; CDW: Changjiang dilute water; TC: Tsushima Current; TWC: Taiwan Current; YSCC: Yellow Sea Cold Current; YSWC: Yellow Sea Warm Current.
currents (Cai, 1986; Wang et al., 2003; Sun et al., 2011). Current study supports the speculation (see above). The connection between the Yellow Sea and East China Sea is primarily through the Yellow Sea Coastal Current and the Taiwan Warm Current (Fig. 6). In addition, the E. pacifica living in the south part (the area south of 34°N) of the Yellow Sea and East China Sea are the same genetically populations (Guo, 2002), suggesting that there is connection between the East China Sea and Yellow Sea populations. Although E. pacifica is currently still abundant in the Yellow Sea (Liu, 2002; Sun et al., 2011; Liu et al., 2012), the question arises: why does E. pacifca in the Yellow Sea not return to the East China Sea when temperature in the East China Sea declined with the Yellow Sea Coast Current? For example, both ST and BT in 2004 and 2006 were relatively similar to that recorded in 1959, but abundance level of the E. pacifica was 0.01 ind.m–3 in May 2006 compared to 1.91 ind.m–3 in May 1959 (Table 1). Further study on the connections between the two populations is essential to reveal the reasons why the E. pacifica population in the East China Sea has not recovered. It is well known that many zooplankton species have geographical distributions that correlate to water masses and circulation patterns (Brinton, 1962). It has been suggested that the distribution of E. pacifica in the East China Sea is related to the cold water mass from the Yellow Sea Current (Wang et al., 2003). However, no direct evidence supports a relationship between the distribution of E. pacifica and the cold water mass in the East China Sea because
Declines in Euphausia pacifica abundance
temperatures in the most abundant areas were not different from those with low abundance levels (Fig. 5). The seasonal distribution (low abundance or disappearance in summer) of E. pacifica (Fig. 3) also reflects that there is no cold water mass in the East China Sea in summer (Su and Yuan, 2005). Therefore, the present data collected in 1959 suggest that E. pacifica was probably advected from the survey areas in summer not being present in water masses with high temperature. Furthermore, we could hypothesize that temperature in the area where E. pacifica (the East China Sea population) inhabit during summer may be anomalous due to the regional warming as well, resulting in the disappearance of the population. Data presented in this study indicate that temporal variability of biological processes and identification of the main factors that drive the dynamic change of marine ecosystems may be complex. We believe the decline of E. pacifica abundance in the East China Sea is a regional response to global warming, but to understand the overall impact, additional factors affecting the E. pacifica distribution and abundance need to be investigated in future studies as have been done in the California Current System by the CalCOFI (1957 to present) and IMECOCAL (1997 to present) research programs. ACKNOWLEDGMENTS This study was funded by the National Science Foundation of China (No. 41176131) and the National Key Program for Fundamental Research and Development (Project 973) (No. 2010CB428705).
REFERENCES Beaugrand G, Reid PC (2003) Long-term changes in phytoplankton, zooplankton and salmon related to climate. Glob Change Biol 9: 801–817 Beaugrand G, Reid PC, Ibañez F, Lindley JA, Edwards M (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296: 1692–11694 Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466: 591–596 Brinton E (1962) The distribution of Pacific euphausiids. Bull Scripps Inst Oceanogr 8: 51–270 Brinton E, Townsend AW (2003) Decadal variability in abundances of the dominant euphausiid species in Southern Sectors of the California Current. Deep-Sea Res II 50: 2449–2472 Cai BJ (1978) Taxonomy study on the Euphausiacea (Crustacea) from the South Yellow Sea and East China Sea. Ocean Sci Tech 8: 39–56 Cai BJ (1986) Distribution of the Euphausiids in the Yellow Sea and the East China Sea. Study collection of crustaceans. Science Press, Beijing, pp 140–146 Chen Q-C, Zhang G-X (1983) Study on Euphausiacea in the central and northern parts of the South China Sea. In “Collected Papers on marine biology in the South China Sea” Ed by Morton B, Hong Kong University Press, Beijing, pp 139–171 Chen Y-Q, Shen X-Q (1999) Changes in the Biomass of the East China Sea Ecosystem. In “Large marine ecosystems of the Pacific rim-assessment, sustainability, and management” Ed by Sherman K, Tang Q-S, Blackwell Science, Malden, pp 221–239 Chen M-R, Shi S-H, Shen H-M (2005) The relationship between sea surface temperature and El Niño events. Mar Forec 22: 80–85 Chen H-J, Qi Y-P, Liu G-X (2011) Spatial and temporal variations of macro- and mesozooplankton community in the Huanghai Sea (Yellow Sea) and East China Sea in summer and winter. Acta
141
Oceanol Sin 30: 84–95 Chiba S, Tadokoro K, Sugisak H, Saino T (2006) Effects of decadal climate change on zooplankton over the last 50 years in the western subarctic North Pacific. Glob Change Biol 12: 907–920 Dippner J, Hänninen J, Kuosa H, Vuorinen I (2001) The influence of climatic variability on zooplankton abundance in the Northern Baltic Archipelago Sea (SW Finland). ICES J Mar Sci 58: 569– 578 Falkowski PG, Barber RT, Smetacekv V (1998) Biogeochemical Controls and Feedbacks on Ocean Primary Production. Science 281: 200–206 Gao Q, Xu Z-L (2011) Effect of regional warming on the abundance of Pseudeuphausia sinica Wang et Chen (Euphausiacea) off the Changjiang River (Yangtze River) estuary. Acta Oceanol Sin 30: 122–128 Gómez-Gutiérrez J, Palomares-García R, Gendron D (1995) Community structure of the euphausiid populations along the west coast of Baja California, Mexico, during the weak ENSO 1986– 1987. Mar Ecol Prog Ser 120: 41–51 Gómez-Gutiérrez J, Feinberg LR, Shaw T, Peterson WT (2007) Interannual and geographical variability of the brood size of the euphausiids Euphausia pacifica and Thysanoessa spinifera along the Oregon coast (1999–2004). Deep Sea Res I 54: 2145–2169 Greenstein BJ, Pandolfi JM (2008) Escaping the heat: range of reef coral taxa in costal Western Australia. Glob Change Biol 14: 513–528 Guo D-H (2002) Molecular ecology studies on genetic diversity and differentiation of common krill in China seas. Ph.D. Thesis, Xiamen University Hansen HJ (1915) The Crustacea Euphausiacea of the United States Museum. Proc U.S. Natl Mus 48: 59–114 Hillebrand H, Burgmer T, Biermann E (2012) Running to stand still: temperature effects on species richness, species turnover, and functional community dynamics. Mar Biol 159: 2415–2422 Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15: 56–61 Iguchi N, Ikeda T (1994) Experimental study on brood size, egg hatchability and early development of a Euphasuiil Euphausia pacifica from Toyama Bay, Southern Japan Sea. Jpn Sea Natl Fish Res Inst 44: 49–57 Lavaniegos BE, Ohman MD (2007) Coherence of long-term variations of zooplankton in two sectors of the California Current System. Prog Oceanogr 75: 42–69 Linacre L (2004) Community structure of Euphausiids in the Southern part of the California current during October 1997 (El Niño) and October 1999 (La Niña). CalCOFI Rep 45: 126–135 Liu H-L (2002) Ecological study on the Yellow Sea and the East China Sea. Ph.D. Thesis. Oceanic Institution, Qingdao Liu P, Song H-J, Wang X, Wang Z-L, Pu X-M, Zhu M-Y (2012) Seasonal variability of the zooplankton community in the southwest of the Huanghai Sea (Yellow Sea) Cold Water Mass. Acta Oceanol Sin 31: 127–139 Mackas DL, Thomson RE, Galbraith M (2001) Changes in the zooplankton community of the British Columbia continental margin, 1985–1999, and their covariation with oceanographic conditions. Can J Fish Aquatic Sci 58: 685–702 Marinovic B, Mangel M (1999) Krill can shrink as an ecological adaptation to temporally unfavorable conditions. Ecol Lett 2: 338–243 Molinero JK, Ibanez F, Souissi S, Buecher E, Dallot S, Nival P (2008) Climate control on the long-term anomalous changes of zooplankton communities in the Northwestern Mediterranean. Glob Change Biol 14: 11–26 Nemoto T (1957) Foods of baleen whales in the northern Pacific. Sci Rep Whales Res Inst 12: 33–90 Ning X-R, Jiang J-X (1991) Marine atlas of Bohai Sea, Yellow Sea
142
Z.-L. Xu and D. Zhang
and East China Sea: Biology. China Ocean Press, Beijing (in Chinese) Ogi H, Tanaka H (1984) Distribution and feeding of the typical sea birds in the subarctic zone of the North Pacific. Gekkan Kaiyo 16: 205–211 Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42 Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308: 1912–1915 Rebstock G (2002) Climatic regime shifts and decadal-scale variability in calanoid copepod populations off southern California. Glob Change Biol 8: 71–89 Richardson AJ, Schoeman DJ (2004) Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305: 1609–1612 Roemmich D, McGowan J (1995) Climate warming and the decline of zooplankton in the California current. Science 267: 1324–1325 Su J-N, Yuan Y-L (2005) Hydrology of China coastal waters. China Ocean Press, Beijing (in Chinese) Sun S, Tao Z-C, Li C-L, Liu H-L (2011) Spatial distribution and population structure of Euphausia pacifica in the Yellow Sea (2006–2007). J Plankton Res 33: 873–889 Tanasichuk RW (1998) Interannual variation in the population biology and productivity of Euphausia pacifica in Barkely Sound, Canada, with special reference to the 1992 and 1993 warm ocean years. Mar Ecol Prog Ser 173: 163–180 Tanasichuk RW, Ware DM, Shaw W, McFarlane GA (1991) Varia-
tion in the diet, daily ration and feeding periodicity of Pacific hake (Merluccius productus) and spiny dogfish (Squalus acanthias) off the lower west coast of Vancouver Island. Can J Fish Aquatic Sci 48: 2118–2128 Tu J-B, Wang B-D (2006) Assessment of eutrophication status in the Changjiang River estuary and its adjacent waters. Adv Mar Sci 24: 532–538 Walther G, Post E, Convey P, Menzel A, Parmesanll C, Beebee TJC, et al. (2002) Ecological responses to recent climate change. Nature 416: 389–395 Wang R, Chen Y-Q, Zuo T, Wang K (2003) Quantitative distribution of euphausiieds in the Yellow Sea and the East China Sea in spring and autumn in relation to the hydrographic conditions. J Fish Chn 27 (suppl.): 31–38 Wu Y-M, Xu Z-L, Fan W, Chui X-S (2011) Change of sea surface temperature in the East Chian Sea during 1985–2005. Acta Oceanol Sin 33: 9–18 Xu Z-L (2007) Distribution patterns of pelagic euphausiids in the East China Sea. Acta Ecol Sin 27: 1–9 Yamamura O, Inada T, Shimazaki K (1998) Predation on Euphausia pacifica by demersal fshes: predation impact and influence of physical variability. Mar Biol 132: 185–208 Yoon WD, Cho SH, Lim D, Choi YK, Lee Y (2000) Spatial distribution of Euphausia pacifica (Euphausiacea: Crustacea) in the Yellow Sea. J Plankton Res 22: 939–949 (Received August 2, 2013 / Accepted November 15, 2013)
