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Potential impact of rising seawater temperature on copepods due to coastal power plants in subtropical areas
Journal of Experimental Marine Biology and Ecology 368 (2009) 196–201
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Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
Potential impact of rising seawater temperature on copepods due to coastal power plants in subtropical areas Zhi-Bing Jiang a, Jiang-Ning Zeng a,b, Quan-Zhen Chen a,⁎, Yi-Jun Huang a, Yi-Bo Liao a, Xiao-Qun Xu a, Ping Zheng b a b
Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, 310012, Hangzhou, China College of Environmental and Resource Science, Zhejiang University, 310029, Hangzhou, China
a r t i c l e
i n f o
Article history: Received 17 April 2008 Received in revised form 14 October 2008 Accepted 14 October 2008 Keywords: Cooling water of coastal power plant Critical thermal maximum (CTMax) Marine copepods Temperature increase Thermal tolerance Upper incipient lethal temperature (UILT)
a b s t r a c t The major objective of this study is to understand the upper thermal limits and potential impact of temperature elevation on copepods caused by coastal power plants. Laboratory experiments were designed to evaluate the upper incipient lethal temperature (UILT) and critical thermal maximum (CTMax) of eight coastal copepod species collected from a subtropical bay in spring and summer. The 48h-UILT of copepods acclimatized at 16.0, 20.0, 28.0 °C were 26.4–29.1, 27.3–30.1, 32.9–36.9 °C, respectively. And the CTMax of copepods acclimatized at 28.0 °C was 35.80–41.03 °C. The UILT of copepods increased significantly with rising acclimatization temperatures, but the difference values between UILT and acclimatization temperatures decreased, which indicated that the seawater temperature elevation induced the growing mortalities of copepods with increasing natural seawater temperatures from the thermal addition of power plants. The results also showed that estuarine copepods had more tolerances to the thermal stress than those from other more stable marine environments. As to the calanoid copepod species, there was a significant negative correlation between the CTMax and body length (p b 0.01). So it seemed that the copepod species with large body size were more sensitive to the thermal addition than the smaller ones. Thus, owing to the temperature increase, the copepod species diversity might reduce and the composition of copepod communities might tend to be small-sized in natural sea areas close to the coastal power plants. © 2008 Elsevier B.V. All rights reserved.
1. Introduction In the process of generating electricity, many coastal fuel (fossil fuels or nuclear reactors) power plants rely on seawater for cooling their condensers. The efficiency of power stations is generally 40–45% which results in a large amount of waste heat rejecting into the marine environment (Bamber, 1995). So the seawater, together with the marine plankton, is drawn into the cooling circuits where the organisms are subjected to an acute thermal shock, at a temperature increment of 6–12 °C above ambient (Bamber, 1995; Martínez-Arroyo et al., 2000; Thiyagarajan et al., 2000; Hoffmeyer et al., 2005; Poornima et al., 2006). Subsequently, this cooling water is released back to the environment which causes temperature increase in receiving sea areas. A 1800–2000 MW direct-cooled power station may use the order of 60 m3 s- 1 of cooling water (Bamber and Seaby, 2004). Since
⁎ Corresponding author. Present address: Second Institute of Oceanography, State Oceanic Administration, No.36 Baocu Northern Road, 310012, Hangzhou, China. Tel.: +86 571 88076924x2386; fax: +86 571 88071539. E-mail address: [email protected] (Q.-Z. Chen). 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.10.016
temperature is a very important ecological parameter, such vast quantities of thermal waters can affect marine organisms as well as their community structure and ecosystem (Langford, 1990; Hung et al., 1998; Schiel et al., 2004; Contador, 2005). Moreover, elevated seawater temperature caused by the global warming (Smith and Reynolds, 2005) may aggravate the impact of thermal pollution on plankton in cooling systems and receiving waters, and this can overwhelm the capacities of many species to tolerance (Zargar and Ghosh, 2007). Thus, the increased demand for coastal power plants has been complemented by a growing concern over the potential negative impact of plankton in associated cooling waters. Among marine plankton, copepods represent the major group of the second producer who plays a key role in the cycling of nutrients and energy in marine ecosystem by forming a trophodynamic link between primary (e.g. phytoplankton) and tertiary (e.g. planktivorous fish) production (De-Young et al., 2004). Several researchers have reported the impact of temperature increase on copepods due to power plants (Alden, 1979; Suresh et al., 1996; Hung et al., 1998; Guseva and Chebotina, 2001; Yang et al., 2002; Hwang et al., 2004; Hoffmeyer et al., 2005). However, very little work has ever been performed on the thermal limits of copepods (González, 1974; Bradley, 1978; Lahdes, 1995). So the present information is not enough to
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predict whether the temperature elevation exceeds the thermal tolerance levels of copepod species in cooling systems and receiving waters close to power plants. Therefore, it is necessary to study the temperature tolerance limits of dominant copepod species. In addition, the temperature increase caused by coastal power plants should be restricted in cooling systems and receiving waters, and the criteria of seawater temperature increment should be formulated according to the thermal limits of marine organisms, such as copepods, for realizing the balance between the full usage of seawater resource and environmental protection. Thus, it is critical to study the thermal tolerance of dominant copepods in different sea areas. Experimental determination of the organisms’ thermal tolerances is a common practice in the field of thermal biology (Mora and Maya, 2006). Two methodologies have been generally used to estimate upper thermal tolerance limits of animals (Beitinger and Bennett, 2000; Galbreath et al., 2004; Hopkin et al., 2006; Mora and Maya, 2006). In the static method, the upper incipient lethal temperature (UILT) which causes 50% mortality is determined from a plot percent mortality at static temperatures, whereas in the dynamic method, critical thermal maximum (CTMax) is the temperature which increases gradually till a critical point. To understand the upper thermal limits and potential impact of temperature elevation on copepods due to coastal power plants, the laboratory experiments on UILT and CTMax of eight coastal copepod species in a subtropical bay were carried out. The results would be more useful to the ecological evaluation and regulation formulation of temperature increase in cooling systems and receiving waters.
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2. Materials and methods 2.1. Sampling collection and maintenance The experimental copepods of the following species were collected with a mesh silk (505 μm) in the Yueqingwan Bay (28°39′N, 121°23′E), Zhejiang Province, China (Fig. 1): Acartia pacifica (Steuer), Acartia spinicauda (Giesbrecht), Calanopia thompsoni (A. Scott), Calanus sinicus (Brodsky), Centropages dorsispinatus (Thompson & Scott), Euchaeta concinna (Dana), Labidocera euchaeta (Giesbrecht), and Pseudodiaptomus marinus (Sato). At each sampling time (04/2007, 05/2007 and 08/ 2007), the natural water temperatures were 16.0, 20.0 and 28.0 °C, respectively. Samples were stored in several 40-l aerated isotherm tanks and transported to the laboratory at once. Then animals were placed into a 2000-l tank filled with aerated filtered seawater (20–25 psu) and maintained at the natural temperature for 2 days. During this time, they were fed on the microalga Isochrysis galbana. And the fresheaters were also fed on the small copepods such as Paracalanus parvus and P. aculeatus. Culture containers were exposed to identical lighting condition with 500 ± 50 lux in a 16 h : 8 h light and dark cycle. After 48 h of maintenance, species were sorted out by a pipette and acclimated for 12 h in several 2-l beakers containing prepared water to allow acclimation prior to experiment (120 adult individuals/beakers). 2.2. UILT experiment To discover the ranges of temperature tolerances of experimental copepods, preliminary tests were performed. Different temperature
Fig. 1. Map of the Yueqingwan Bay, southern Zhejiang Province, China, showing the location of sample station.
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Table 1 UILT of different copepod species under different acclimatization temperatures Species
Ecological association
A. pacifica A. spinicauda C. dorsispinatus C. sinicus
Coastal Coastal Coastal Coastal
low-salinity species association low-salinity species association low-salinity species association warm-temperate species association
C. thompsoni E. concinna
Coastal low-salinity species association Cosmopolitan warm-water species association
L. euchaeta
Coastal low-salinity species association
P. marinus
Estuarine brackish species association
Acclimatization temperature (°C) 28.0 28.0 20.0 16.0 20.0 28.0 16.0 20.0 16.0 20.0 28.0 28.0
24h-UILT
48h-UILT
(°C)
(°C)
35.0 (34.6–35.6) 35.4 (35.0–35.8) 29.6 (29.3–29.9) 26.9 (26.8–27.0) 27.7 (27.6–27.8) 33.9 (33.7–34.0) 28.2 (28.0–28.3) 29.1 (28.9–29.2) 30.0 (29.7–30.3) 31.0 (30.8–31.3) 34.0 (33.8–34.2) 37.4 (37.3–37.6)
34.4 (33.8–34.9) 35.2 (34.9–35.6) 29.2 (29.0–29.5) 26.4 (26.3–26.5) 27.3 (27.2–27.4) 32.9 (32.7–33.1) 27.7 (27.4–27.8) 28.6 (28.5–28.7) 29.1 (28.8–29.4) 30.1 (29.8–30.3) 33.1 (32.9–33.3) 36.9 (36.8–37.0)
Values in brackets after the UILT values indicated their 95% confidence limits.
gradients were prepared for different species according to the preliminary tests. To avoid the thermal stress by abrupt transfer, 20 healthy adult copepods from 2-l beakers were transferred in a small volume of water to each 500-ml glass jar containing 400 ml of filtered water at the acclimatization temperature. Then the glass jars were placed into the bath (50-l tank) for bathing where the water temperature increased at a constant rate of 0.1 °C min-1. Experimental animals were exposed for 48 h to the water temperature at the scheduled temperature gradient. Each bath was equipped with an electronic temperature control, a temperature sensor (WMZK-01) and a 300 W heater with the accuracy of 0.2 °C. Each bath was aerated to keep the water temperature uniform. The glass jars were also gently aerated for maintaining the oxygen tension at a constant level. Control animals were similarly treated without heating. Experiments were run in triplicate. The mortality of copepods was observed at an interval of 1, 6, 12, 24, 48 h. Criterion for the death was reached if no reactivity was detected when the animals were gently touched for 15 s. 2.3. CTMax experiment 50-ml glass jar containing 5 healthy adult copepods in 40 ml water was transferred to a temperature controlled bath at their acclimatization temperature (28.0 °C). The temperature of bath increased constantly at the rate of 0.33 °C min- 1 until the critical point was reached. It is only necessary to observe the water temperature change during the experiment, since they are too small and the temperature of their entire body changes is parallel to water temperature changes (González, 1974). Control copepods were same treated without heating. Experiments were run in triplicate. The critical point was quantified as the mean temperature when an individual copepod showed no reactivity by being gently touched with a pipette. At the end of this experiment, body length of 15 test individuals of each copepod species were measured by the optical microscope (Leica MZ16).
cantly with increasing exposure duration. For the same species, the 48h-UILT were significantly lower than the 24h-UILT except C. dorsispinatus (Table 1). Thermal tolerance of the same copepod species increased significantly with rising acclimatization temperature (Table 1). For example, the 48h-UILT of C. sinicus and E. concinna acclimatized at 20 °C (27.3 and 28.6 °C, respectively) were significantly higher than the organisms acclimatized at 16 °C (26.4 and 27.7 °C, respectively); the 48h-UILT of L. euchaeta acclimatized at 28 °C (33.1 °C) was significantly higher than the one acclimatized at 20 °C (30.1 °C), and the 48h-UILT of L. euchaeta acclimatized at 20 °C was significantly higher than the one acclimatized at 16 °C (29.1 °C). It could be concluded that the thermal tolerance differences among experimental copepod species were significant at the same exposure time and acclimatization temperature (Table 1). When the acclimatization temperature was 16 °C, the thermal tolerance of L. euchaeta was significantly better than that of E. concinna, and E. concinna was significantly better than C. sinicus. When the acclimatization temperature was 20 °C, the thermal tolerance of L. euchaeta was the maximum among four copepod species; and the thermal tolerance of C. dorsispinatus was significantly better than E. concinna and C. sinicus. When the acclimatization temperature was 28.0 °C, P. marinu had the highest UILT and C. thompsoni had the lowest UILT. The CTMax ranged from 35.80 to 41.03 °C in seven copepod species acclimatized at 28.0 °C in summer (Table 2). There were no significant differences between C. sinicus (35.80 °C) and E. concinna (35.90 °C) (p N 0.05), as well as L. euchaeta (38.56 °C) and A. pacifica (38.59 °C), but differences among other copepod species were significant (p b 0.05). Table 2 showed that the CTMax of calanoid copepod species increased with decreasing body sizes, and the CTMax of experimental copepod species from the maximum to the minimum were P. marinu, A. spinicauda, L. euchaeta, A. pacifica, C. thompsoni, E. concinna and C. sinicus. There was a significant negative correlation between CTMax
2.4. Data analysis The 24h-UILT, 48h-UILT, and their 95% confidence limits were calculated by SPSS 13.0 according to the probit analysis. The mortalities of control groups were included in the data analysis. The statistical analysis of CTMax experimental result was used by One-way ANOVA and LSD (0.05) multiple comparison test. 3. Results The UILT results among the tests are significantly different since the 95% confidence limits of UILT did not overlap. So the results showed that the thermal tolerance of copepods decreased signifi-
Table 2 CTMax and body length of different copepod species acclimatized at 28.0 °C Species
Body length ± SE (mm)
CTMax ± SE (°C)
A. pacifica A. spinicauda C. thompsoni C. sinicus E. concinna L. euchaeta P. marinus
1.26 ± 0.04 1.19 ± 0.03 1.87 ± 0.03 2.95 ± 0.05 2.74 ± 0.04 2.35 ± 0.06 1.09 ± 0.04
38.59 ± 0.11c 39.53 ± 0.08d 38.19 ± 0.14b 35.80 ± 0.09a 35.90 ± 0.10a 38.56 ± 0.11c 41.03 ± 0.09e
SE = standard error of the mean. The CTMax values followed by different letters were significant at level of 0.05, LSD multiple comparison tests were used.
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CTMax experiments in spring and summer, as it is a warm-temperate species and adapts to lower temperature in natural circumstances (Wang et al., 2003; Zhang et al., 2007). Whereas, P. marinu is a typical estuarine species which can be responsible for its maximum thermal tolerance. Generally, estuarine species usually show higher tolerances to the thermal stress than those from other more stable marine environments, owing to their eurythermic characteristics (Hoffmeyer et al., 2005). Alden (1979) considered that the estuarine species had apparently evolved the ability to live in subtropical areas under temperature conditions much closer to their upper thermal limits. 4.2. Potential impact of temperature increase on copepods from coastal power plants Fig. 2. Relationship between the CTMax and body size of experimental copepod species.
and body length of the experimental copepod species (r = 0.89, p b 0.01) (Fig. 2). 4. Discussion 4.1. Thermal tolerance of marine copepods Temperature is one of the most important environmental parameters since it determines the living area (Pörtner, 2001, 2002; Beaugrand et al., 2002) and affects the spawning, reproduction, development, growth, metabolism, feeding, and behavior of copepods (Gaudy et al., 2000; Halsband-Lenk et al., 2002; Devreker et al., 2004; Holste and Peck, 2006; Lagerspetz and Vainio, 2006). Copepods can adapt themselves to the moderate changing temperature, but mortality would be observed if the temperature increase exceeds their bearing capacity. The experimental copepods were collected from natural sea area, and the samples were selected randomly during the experiment. So the ratios of male and female of copepods were according with the animals in natural condition. Though these ratios varied with the species of copepods, they reflected the fact in natural sea area. Therefore, it was unnecessary to separate the male and female from the experimental animals (González, 1974; Lahdes, 1995; Jiang et al., 2008). Many organisms can tolerate extreme temperatures in short time by adjusting their physical mechanisms under the thermal stress (Jiang et al., 2008), such as support of anaerobic metabolism, functions of heat shock proteins, and antioxidative defence (Pörtner, 2002; Voznesensky et al., 2004). For example, the paper of Lahdes (1995) showed that the lethal temperature of Calanoides acutus exposed for 15 min was 18.1 °C. When the exposure duration prolonged to 12 h, the thermal limit of C. acutus was 14.3 °C, which decreased significantly. Also, in this work, the thermal tolerances of copepods decreased with increasing exposure time (Table 1). In this study, the thermal tolerance of experimental copepods (e.g., C. sinicus, E. concinna, and L. euchaeta) increased with rising acclimatization temperature, which was in agreement with the earlier studies on the thermal tolerance of Acartia tonsa and A. clause (González, 1974). Besides, thermal tolerance ranges can also be extended through the induction of heat shock proteins (hsps) (Somero, 1995). In the experiments of Frankenberg et al. (2000) and Voznesensky et al. (2004), the hsp 70 levels of Artemia franciscana and Calanus finmarchicus could be elevated by short-term thermal shock. Thermal tolerances of organisms are resulted from long-term natural selection and evolution under environmental function. Thermal windows vary widely among species, and the organisms adapt to higher temperature which thermal tolerance is better than the ones that prefer to lower temperature (Somero, 1995; Pörtner, 2001). In this work, C. sinicus was the most sensitive one to the thermal stress among these copepod species during the UILT and
Much attention is paid to the potential environmental impact of elevated temperature seawater on marine organisms and the ecosystem, which has become one of the foremost problems during the risk assessment of coastal power plant development and future planning. Many researches have been done about the influence of temperature increase due to coastal power plants on bacteria (Choi et al., 2002; Shiah et al., 2005), phytoplankton (Martínez-Arroyo et al., 2000; Lo et al., 2004; Poornima et al., 2005, 2006), fishes (Rajaguru and Ramachandran, 2001; Rajaguru, 2002), crabs (Suresh et al., 1995), sedentary organisms (Suresh et al, 1993; Lardicci et al. 1999; Schiel et al., 2004), copepods (Alden, 1979; Suresh et al., 1996; Hwang et al., 2004), and other zooplankton (Mahyew et al., 2000; Melton and Serviss, 2000; Yang et al., 2002). It is reported that the seawater temperature increases about 6– 10 °C in cooling systems in tropical zones (Martínez-Arroyo et al., 2000; Thiyagarajan et al., 2000; Poornima et al., 2006), and 8–12 °C in temperate areas (Bamber, 1995; Bamber and Seaby, 2004; Hoffmeyer et al., 2005). According to the experimental results, the temperature increments caused by coastal power plants approach or even exceed the thermal limits of most coastal copepod species (Tables 1 and 2). As a result, the thermal sensitivity of marine copepods to thermal stress could be of great significance in limiting the distribution and abundance of copepods in subtropical areas. This is congruent with the conclusion of Alden (1979). Copepods float easily into the high elevated temperature waters near outfalls because of the outside forces, such as ocean currents, tidal currents, and stormy waves. Consequently, injury or induced mortality of marine copepods may be a result of thermal stress due to their ambient water temperature approaching or even exceeding their UILT and CTMax. In fact, the impact of thermal effluent on copepods is more severe in the bay or harbor where temperature elevated water can not exchange or diffuse in time. Suresh et al. (1996) found that the density of the copepods drastically reduced in high temperature waters near the discharge, while the population of copepods restored in all areas near the outfall when the power plant shutdown and the
Fig. 3. Difference values between 48h-UILT and acclimatization temperatures of copepods under different acclimatization temperatures.
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normal water temperatures prevailed again. So the mortalitiy or disappearance of most copepod species may occur if the temperature increment goes beyond their adaptive temperature ranges. The difference values between UILT and acclimatization temperature of copepods decreased with rising acclimatization temperatures (Fig. 3), which indicated that the mortalities of marine copepods due to the thermal stress of power plants increased with elevated acclimatization temperatures. The investigations made by Alden (1979) and Hoffmeyer et al. (2005) proved this deduction. The former reported that mass copepods mortality occurred due to the thermal discharge from the power plant located in a subtropical estuary during the warmest months of the year. And the latter revealed that the highest mortality of A. tonsa took place in the middle of summer and the lowest mortality in winter in a power plant cooling system. Species react differently to the thermal stress caused by coastal power plants in accordance with their degrees of acclimation to natural temperature variations and their tolerance ranges (Hoffmeyer et al., 2005). During the CTMax experiment, it seemed that the thermal sensitivity of calanoid copepod species enhanced with the increase of their particle sizes (Table 2 and Fig. 2). Recently, owing to the changing climate, researchers reported the shift from larger (C. finmarchicus) to smaller (C. helgolandicus) copepod fauna in the North Sea under the seawater temperature increase (Beaugrand and Reid, 2003; Beaugrand et al., 2003). And this was largely determined by different thermal windows of the two copepod species (Helaouët and Beaugrand, 2007). Similarly, the number and abundance of those meso- and macro-copepod species sensitive to the thermal stress might decrease due to coastal power plants. Contrarily, microcopepod species tolerant to the thermal addition might become the dominant species or their dominances increase. In consequence, the species diversity reduced and the composition of copepod communities tended to be small-sized. Finally, a disturbed and degenerate marine ecosystem near coastal power plants might be a result of the structure and function change of copepod community. 5. Conclusion It can be concluded that the UILT and CTMax of eight coastal copepod species were related to the particle sizes, geographical distributions, seasons, and acclimatization temperatures. Based on the data obtained in this study, the temperature increase seemed to approach or even exceed the thermal tolerance levels of most copepod species due to coastal power plants, especially in the warm months. Since marine copepods are sensitive to the thermal stress, the rising seawater temperature caused by coastal power plants can be of great significance in limiting the distributions and abundances of them in subtropical zones. Besides, the great variations of thermal sensitivities among copepod species to heat stress might lead to an abnormal community succession in natural environment near the power plants. So the results would be more useful to formulate the regulation and evaluate ecological effect of temperature increase in cooling systems and receiving waters. However, besides the problem caused by the elevated temperature, the biocides (e.g. chlorine), widely introduced as antifouling agent in cooling water (Capuzzo, 1980; Bamber and Seaby, 2004; Taylor, 2006; Zargar and Ghosh, 2007), might also affect the copepods. More researches should be conducted to examine the thermal limits of dominant copepods in different regions, and further work should be required to assess the long-term response of the copepod community under the thermal and biocidal addition of coastal power plants. Acknowledgements We thank Qi-Lang Xie, Xue-Liang Cai, and Jin-He Zheng etc. at Zhejiang Mariculture Research Institute for supports and facilities. We also thank Suzanne Bricker for the constructive comments. This work was supported by the Program on Research for Public Good of the Ministry of Science and Technology of the People’s Republic of China
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Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
Potential impact of rising seawater temperature on copepods due to coastal power plants in subtropical areas Zhi-Bing Jiang a, Jiang-Ning Zeng a,b, Quan-Zhen Chen a,⁎, Yi-Jun Huang a, Yi-Bo Liao a, Xiao-Qun Xu a, Ping Zheng b a b
Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, 310012, Hangzhou, China College of Environmental and Resource Science, Zhejiang University, 310029, Hangzhou, China
a r t i c l e
i n f o
Article history: Received 17 April 2008 Received in revised form 14 October 2008 Accepted 14 October 2008 Keywords: Cooling water of coastal power plant Critical thermal maximum (CTMax) Marine copepods Temperature increase Thermal tolerance Upper incipient lethal temperature (UILT)
a b s t r a c t The major objective of this study is to understand the upper thermal limits and potential impact of temperature elevation on copepods caused by coastal power plants. Laboratory experiments were designed to evaluate the upper incipient lethal temperature (UILT) and critical thermal maximum (CTMax) of eight coastal copepod species collected from a subtropical bay in spring and summer. The 48h-UILT of copepods acclimatized at 16.0, 20.0, 28.0 °C were 26.4–29.1, 27.3–30.1, 32.9–36.9 °C, respectively. And the CTMax of copepods acclimatized at 28.0 °C was 35.80–41.03 °C. The UILT of copepods increased significantly with rising acclimatization temperatures, but the difference values between UILT and acclimatization temperatures decreased, which indicated that the seawater temperature elevation induced the growing mortalities of copepods with increasing natural seawater temperatures from the thermal addition of power plants. The results also showed that estuarine copepods had more tolerances to the thermal stress than those from other more stable marine environments. As to the calanoid copepod species, there was a significant negative correlation between the CTMax and body length (p b 0.01). So it seemed that the copepod species with large body size were more sensitive to the thermal addition than the smaller ones. Thus, owing to the temperature increase, the copepod species diversity might reduce and the composition of copepod communities might tend to be small-sized in natural sea areas close to the coastal power plants. © 2008 Elsevier B.V. All rights reserved.
1. Introduction In the process of generating electricity, many coastal fuel (fossil fuels or nuclear reactors) power plants rely on seawater for cooling their condensers. The efficiency of power stations is generally 40–45% which results in a large amount of waste heat rejecting into the marine environment (Bamber, 1995). So the seawater, together with the marine plankton, is drawn into the cooling circuits where the organisms are subjected to an acute thermal shock, at a temperature increment of 6–12 °C above ambient (Bamber, 1995; Martínez-Arroyo et al., 2000; Thiyagarajan et al., 2000; Hoffmeyer et al., 2005; Poornima et al., 2006). Subsequently, this cooling water is released back to the environment which causes temperature increase in receiving sea areas. A 1800–2000 MW direct-cooled power station may use the order of 60 m3 s- 1 of cooling water (Bamber and Seaby, 2004). Since
⁎ Corresponding author. Present address: Second Institute of Oceanography, State Oceanic Administration, No.36 Baocu Northern Road, 310012, Hangzhou, China. Tel.: +86 571 88076924x2386; fax: +86 571 88071539. E-mail address: [email protected] (Q.-Z. Chen). 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.10.016
temperature is a very important ecological parameter, such vast quantities of thermal waters can affect marine organisms as well as their community structure and ecosystem (Langford, 1990; Hung et al., 1998; Schiel et al., 2004; Contador, 2005). Moreover, elevated seawater temperature caused by the global warming (Smith and Reynolds, 2005) may aggravate the impact of thermal pollution on plankton in cooling systems and receiving waters, and this can overwhelm the capacities of many species to tolerance (Zargar and Ghosh, 2007). Thus, the increased demand for coastal power plants has been complemented by a growing concern over the potential negative impact of plankton in associated cooling waters. Among marine plankton, copepods represent the major group of the second producer who plays a key role in the cycling of nutrients and energy in marine ecosystem by forming a trophodynamic link between primary (e.g. phytoplankton) and tertiary (e.g. planktivorous fish) production (De-Young et al., 2004). Several researchers have reported the impact of temperature increase on copepods due to power plants (Alden, 1979; Suresh et al., 1996; Hung et al., 1998; Guseva and Chebotina, 2001; Yang et al., 2002; Hwang et al., 2004; Hoffmeyer et al., 2005). However, very little work has ever been performed on the thermal limits of copepods (González, 1974; Bradley, 1978; Lahdes, 1995). So the present information is not enough to
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predict whether the temperature elevation exceeds the thermal tolerance levels of copepod species in cooling systems and receiving waters close to power plants. Therefore, it is necessary to study the temperature tolerance limits of dominant copepod species. In addition, the temperature increase caused by coastal power plants should be restricted in cooling systems and receiving waters, and the criteria of seawater temperature increment should be formulated according to the thermal limits of marine organisms, such as copepods, for realizing the balance between the full usage of seawater resource and environmental protection. Thus, it is critical to study the thermal tolerance of dominant copepods in different sea areas. Experimental determination of the organisms’ thermal tolerances is a common practice in the field of thermal biology (Mora and Maya, 2006). Two methodologies have been generally used to estimate upper thermal tolerance limits of animals (Beitinger and Bennett, 2000; Galbreath et al., 2004; Hopkin et al., 2006; Mora and Maya, 2006). In the static method, the upper incipient lethal temperature (UILT) which causes 50% mortality is determined from a plot percent mortality at static temperatures, whereas in the dynamic method, critical thermal maximum (CTMax) is the temperature which increases gradually till a critical point. To understand the upper thermal limits and potential impact of temperature elevation on copepods due to coastal power plants, the laboratory experiments on UILT and CTMax of eight coastal copepod species in a subtropical bay were carried out. The results would be more useful to the ecological evaluation and regulation formulation of temperature increase in cooling systems and receiving waters.
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2. Materials and methods 2.1. Sampling collection and maintenance The experimental copepods of the following species were collected with a mesh silk (505 μm) in the Yueqingwan Bay (28°39′N, 121°23′E), Zhejiang Province, China (Fig. 1): Acartia pacifica (Steuer), Acartia spinicauda (Giesbrecht), Calanopia thompsoni (A. Scott), Calanus sinicus (Brodsky), Centropages dorsispinatus (Thompson & Scott), Euchaeta concinna (Dana), Labidocera euchaeta (Giesbrecht), and Pseudodiaptomus marinus (Sato). At each sampling time (04/2007, 05/2007 and 08/ 2007), the natural water temperatures were 16.0, 20.0 and 28.0 °C, respectively. Samples were stored in several 40-l aerated isotherm tanks and transported to the laboratory at once. Then animals were placed into a 2000-l tank filled with aerated filtered seawater (20–25 psu) and maintained at the natural temperature for 2 days. During this time, they were fed on the microalga Isochrysis galbana. And the fresheaters were also fed on the small copepods such as Paracalanus parvus and P. aculeatus. Culture containers were exposed to identical lighting condition with 500 ± 50 lux in a 16 h : 8 h light and dark cycle. After 48 h of maintenance, species were sorted out by a pipette and acclimated for 12 h in several 2-l beakers containing prepared water to allow acclimation prior to experiment (120 adult individuals/beakers). 2.2. UILT experiment To discover the ranges of temperature tolerances of experimental copepods, preliminary tests were performed. Different temperature
Fig. 1. Map of the Yueqingwan Bay, southern Zhejiang Province, China, showing the location of sample station.
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Table 1 UILT of different copepod species under different acclimatization temperatures Species
Ecological association
A. pacifica A. spinicauda C. dorsispinatus C. sinicus
Coastal Coastal Coastal Coastal
low-salinity species association low-salinity species association low-salinity species association warm-temperate species association
C. thompsoni E. concinna
Coastal low-salinity species association Cosmopolitan warm-water species association
L. euchaeta
Coastal low-salinity species association
P. marinus
Estuarine brackish species association
Acclimatization temperature (°C) 28.0 28.0 20.0 16.0 20.0 28.0 16.0 20.0 16.0 20.0 28.0 28.0
24h-UILT
48h-UILT
(°C)
(°C)
35.0 (34.6–35.6) 35.4 (35.0–35.8) 29.6 (29.3–29.9) 26.9 (26.8–27.0) 27.7 (27.6–27.8) 33.9 (33.7–34.0) 28.2 (28.0–28.3) 29.1 (28.9–29.2) 30.0 (29.7–30.3) 31.0 (30.8–31.3) 34.0 (33.8–34.2) 37.4 (37.3–37.6)
34.4 (33.8–34.9) 35.2 (34.9–35.6) 29.2 (29.0–29.5) 26.4 (26.3–26.5) 27.3 (27.2–27.4) 32.9 (32.7–33.1) 27.7 (27.4–27.8) 28.6 (28.5–28.7) 29.1 (28.8–29.4) 30.1 (29.8–30.3) 33.1 (32.9–33.3) 36.9 (36.8–37.0)
Values in brackets after the UILT values indicated their 95% confidence limits.
gradients were prepared for different species according to the preliminary tests. To avoid the thermal stress by abrupt transfer, 20 healthy adult copepods from 2-l beakers were transferred in a small volume of water to each 500-ml glass jar containing 400 ml of filtered water at the acclimatization temperature. Then the glass jars were placed into the bath (50-l tank) for bathing where the water temperature increased at a constant rate of 0.1 °C min-1. Experimental animals were exposed for 48 h to the water temperature at the scheduled temperature gradient. Each bath was equipped with an electronic temperature control, a temperature sensor (WMZK-01) and a 300 W heater with the accuracy of 0.2 °C. Each bath was aerated to keep the water temperature uniform. The glass jars were also gently aerated for maintaining the oxygen tension at a constant level. Control animals were similarly treated without heating. Experiments were run in triplicate. The mortality of copepods was observed at an interval of 1, 6, 12, 24, 48 h. Criterion for the death was reached if no reactivity was detected when the animals were gently touched for 15 s. 2.3. CTMax experiment 50-ml glass jar containing 5 healthy adult copepods in 40 ml water was transferred to a temperature controlled bath at their acclimatization temperature (28.0 °C). The temperature of bath increased constantly at the rate of 0.33 °C min- 1 until the critical point was reached. It is only necessary to observe the water temperature change during the experiment, since they are too small and the temperature of their entire body changes is parallel to water temperature changes (González, 1974). Control copepods were same treated without heating. Experiments were run in triplicate. The critical point was quantified as the mean temperature when an individual copepod showed no reactivity by being gently touched with a pipette. At the end of this experiment, body length of 15 test individuals of each copepod species were measured by the optical microscope (Leica MZ16).
cantly with increasing exposure duration. For the same species, the 48h-UILT were significantly lower than the 24h-UILT except C. dorsispinatus (Table 1). Thermal tolerance of the same copepod species increased significantly with rising acclimatization temperature (Table 1). For example, the 48h-UILT of C. sinicus and E. concinna acclimatized at 20 °C (27.3 and 28.6 °C, respectively) were significantly higher than the organisms acclimatized at 16 °C (26.4 and 27.7 °C, respectively); the 48h-UILT of L. euchaeta acclimatized at 28 °C (33.1 °C) was significantly higher than the one acclimatized at 20 °C (30.1 °C), and the 48h-UILT of L. euchaeta acclimatized at 20 °C was significantly higher than the one acclimatized at 16 °C (29.1 °C). It could be concluded that the thermal tolerance differences among experimental copepod species were significant at the same exposure time and acclimatization temperature (Table 1). When the acclimatization temperature was 16 °C, the thermal tolerance of L. euchaeta was significantly better than that of E. concinna, and E. concinna was significantly better than C. sinicus. When the acclimatization temperature was 20 °C, the thermal tolerance of L. euchaeta was the maximum among four copepod species; and the thermal tolerance of C. dorsispinatus was significantly better than E. concinna and C. sinicus. When the acclimatization temperature was 28.0 °C, P. marinu had the highest UILT and C. thompsoni had the lowest UILT. The CTMax ranged from 35.80 to 41.03 °C in seven copepod species acclimatized at 28.0 °C in summer (Table 2). There were no significant differences between C. sinicus (35.80 °C) and E. concinna (35.90 °C) (p N 0.05), as well as L. euchaeta (38.56 °C) and A. pacifica (38.59 °C), but differences among other copepod species were significant (p b 0.05). Table 2 showed that the CTMax of calanoid copepod species increased with decreasing body sizes, and the CTMax of experimental copepod species from the maximum to the minimum were P. marinu, A. spinicauda, L. euchaeta, A. pacifica, C. thompsoni, E. concinna and C. sinicus. There was a significant negative correlation between CTMax
2.4. Data analysis The 24h-UILT, 48h-UILT, and their 95% confidence limits were calculated by SPSS 13.0 according to the probit analysis. The mortalities of control groups were included in the data analysis. The statistical analysis of CTMax experimental result was used by One-way ANOVA and LSD (0.05) multiple comparison test. 3. Results The UILT results among the tests are significantly different since the 95% confidence limits of UILT did not overlap. So the results showed that the thermal tolerance of copepods decreased signifi-
Table 2 CTMax and body length of different copepod species acclimatized at 28.0 °C Species
Body length ± SE (mm)
CTMax ± SE (°C)
A. pacifica A. spinicauda C. thompsoni C. sinicus E. concinna L. euchaeta P. marinus
1.26 ± 0.04 1.19 ± 0.03 1.87 ± 0.03 2.95 ± 0.05 2.74 ± 0.04 2.35 ± 0.06 1.09 ± 0.04
38.59 ± 0.11c 39.53 ± 0.08d 38.19 ± 0.14b 35.80 ± 0.09a 35.90 ± 0.10a 38.56 ± 0.11c 41.03 ± 0.09e
SE = standard error of the mean. The CTMax values followed by different letters were significant at level of 0.05, LSD multiple comparison tests were used.
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CTMax experiments in spring and summer, as it is a warm-temperate species and adapts to lower temperature in natural circumstances (Wang et al., 2003; Zhang et al., 2007). Whereas, P. marinu is a typical estuarine species which can be responsible for its maximum thermal tolerance. Generally, estuarine species usually show higher tolerances to the thermal stress than those from other more stable marine environments, owing to their eurythermic characteristics (Hoffmeyer et al., 2005). Alden (1979) considered that the estuarine species had apparently evolved the ability to live in subtropical areas under temperature conditions much closer to their upper thermal limits. 4.2. Potential impact of temperature increase on copepods from coastal power plants Fig. 2. Relationship between the CTMax and body size of experimental copepod species.
and body length of the experimental copepod species (r = 0.89, p b 0.01) (Fig. 2). 4. Discussion 4.1. Thermal tolerance of marine copepods Temperature is one of the most important environmental parameters since it determines the living area (Pörtner, 2001, 2002; Beaugrand et al., 2002) and affects the spawning, reproduction, development, growth, metabolism, feeding, and behavior of copepods (Gaudy et al., 2000; Halsband-Lenk et al., 2002; Devreker et al., 2004; Holste and Peck, 2006; Lagerspetz and Vainio, 2006). Copepods can adapt themselves to the moderate changing temperature, but mortality would be observed if the temperature increase exceeds their bearing capacity. The experimental copepods were collected from natural sea area, and the samples were selected randomly during the experiment. So the ratios of male and female of copepods were according with the animals in natural condition. Though these ratios varied with the species of copepods, they reflected the fact in natural sea area. Therefore, it was unnecessary to separate the male and female from the experimental animals (González, 1974; Lahdes, 1995; Jiang et al., 2008). Many organisms can tolerate extreme temperatures in short time by adjusting their physical mechanisms under the thermal stress (Jiang et al., 2008), such as support of anaerobic metabolism, functions of heat shock proteins, and antioxidative defence (Pörtner, 2002; Voznesensky et al., 2004). For example, the paper of Lahdes (1995) showed that the lethal temperature of Calanoides acutus exposed for 15 min was 18.1 °C. When the exposure duration prolonged to 12 h, the thermal limit of C. acutus was 14.3 °C, which decreased significantly. Also, in this work, the thermal tolerances of copepods decreased with increasing exposure time (Table 1). In this study, the thermal tolerance of experimental copepods (e.g., C. sinicus, E. concinna, and L. euchaeta) increased with rising acclimatization temperature, which was in agreement with the earlier studies on the thermal tolerance of Acartia tonsa and A. clause (González, 1974). Besides, thermal tolerance ranges can also be extended through the induction of heat shock proteins (hsps) (Somero, 1995). In the experiments of Frankenberg et al. (2000) and Voznesensky et al. (2004), the hsp 70 levels of Artemia franciscana and Calanus finmarchicus could be elevated by short-term thermal shock. Thermal tolerances of organisms are resulted from long-term natural selection and evolution under environmental function. Thermal windows vary widely among species, and the organisms adapt to higher temperature which thermal tolerance is better than the ones that prefer to lower temperature (Somero, 1995; Pörtner, 2001). In this work, C. sinicus was the most sensitive one to the thermal stress among these copepod species during the UILT and
Much attention is paid to the potential environmental impact of elevated temperature seawater on marine organisms and the ecosystem, which has become one of the foremost problems during the risk assessment of coastal power plant development and future planning. Many researches have been done about the influence of temperature increase due to coastal power plants on bacteria (Choi et al., 2002; Shiah et al., 2005), phytoplankton (Martínez-Arroyo et al., 2000; Lo et al., 2004; Poornima et al., 2005, 2006), fishes (Rajaguru and Ramachandran, 2001; Rajaguru, 2002), crabs (Suresh et al., 1995), sedentary organisms (Suresh et al, 1993; Lardicci et al. 1999; Schiel et al., 2004), copepods (Alden, 1979; Suresh et al., 1996; Hwang et al., 2004), and other zooplankton (Mahyew et al., 2000; Melton and Serviss, 2000; Yang et al., 2002). It is reported that the seawater temperature increases about 6– 10 °C in cooling systems in tropical zones (Martínez-Arroyo et al., 2000; Thiyagarajan et al., 2000; Poornima et al., 2006), and 8–12 °C in temperate areas (Bamber, 1995; Bamber and Seaby, 2004; Hoffmeyer et al., 2005). According to the experimental results, the temperature increments caused by coastal power plants approach or even exceed the thermal limits of most coastal copepod species (Tables 1 and 2). As a result, the thermal sensitivity of marine copepods to thermal stress could be of great significance in limiting the distribution and abundance of copepods in subtropical areas. This is congruent with the conclusion of Alden (1979). Copepods float easily into the high elevated temperature waters near outfalls because of the outside forces, such as ocean currents, tidal currents, and stormy waves. Consequently, injury or induced mortality of marine copepods may be a result of thermal stress due to their ambient water temperature approaching or even exceeding their UILT and CTMax. In fact, the impact of thermal effluent on copepods is more severe in the bay or harbor where temperature elevated water can not exchange or diffuse in time. Suresh et al. (1996) found that the density of the copepods drastically reduced in high temperature waters near the discharge, while the population of copepods restored in all areas near the outfall when the power plant shutdown and the
Fig. 3. Difference values between 48h-UILT and acclimatization temperatures of copepods under different acclimatization temperatures.
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normal water temperatures prevailed again. So the mortalitiy or disappearance of most copepod species may occur if the temperature increment goes beyond their adaptive temperature ranges. The difference values between UILT and acclimatization temperature of copepods decreased with rising acclimatization temperatures (Fig. 3), which indicated that the mortalities of marine copepods due to the thermal stress of power plants increased with elevated acclimatization temperatures. The investigations made by Alden (1979) and Hoffmeyer et al. (2005) proved this deduction. The former reported that mass copepods mortality occurred due to the thermal discharge from the power plant located in a subtropical estuary during the warmest months of the year. And the latter revealed that the highest mortality of A. tonsa took place in the middle of summer and the lowest mortality in winter in a power plant cooling system. Species react differently to the thermal stress caused by coastal power plants in accordance with their degrees of acclimation to natural temperature variations and their tolerance ranges (Hoffmeyer et al., 2005). During the CTMax experiment, it seemed that the thermal sensitivity of calanoid copepod species enhanced with the increase of their particle sizes (Table 2 and Fig. 2). Recently, owing to the changing climate, researchers reported the shift from larger (C. finmarchicus) to smaller (C. helgolandicus) copepod fauna in the North Sea under the seawater temperature increase (Beaugrand and Reid, 2003; Beaugrand et al., 2003). And this was largely determined by different thermal windows of the two copepod species (Helaouët and Beaugrand, 2007). Similarly, the number and abundance of those meso- and macro-copepod species sensitive to the thermal stress might decrease due to coastal power plants. Contrarily, microcopepod species tolerant to the thermal addition might become the dominant species or their dominances increase. In consequence, the species diversity reduced and the composition of copepod communities tended to be small-sized. Finally, a disturbed and degenerate marine ecosystem near coastal power plants might be a result of the structure and function change of copepod community. 5. Conclusion It can be concluded that the UILT and CTMax of eight coastal copepod species were related to the particle sizes, geographical distributions, seasons, and acclimatization temperatures. Based on the data obtained in this study, the temperature increase seemed to approach or even exceed the thermal tolerance levels of most copepod species due to coastal power plants, especially in the warm months. Since marine copepods are sensitive to the thermal stress, the rising seawater temperature caused by coastal power plants can be of great significance in limiting the distributions and abundances of them in subtropical zones. Besides, the great variations of thermal sensitivities among copepod species to heat stress might lead to an abnormal community succession in natural environment near the power plants. So the results would be more useful to formulate the regulation and evaluate ecological effect of temperature increase in cooling systems and receiving waters. However, besides the problem caused by the elevated temperature, the biocides (e.g. chlorine), widely introduced as antifouling agent in cooling water (Capuzzo, 1980; Bamber and Seaby, 2004; Taylor, 2006; Zargar and Ghosh, 2007), might also affect the copepods. More researches should be conducted to examine the thermal limits of dominant copepods in different regions, and further work should be required to assess the long-term response of the copepod community under the thermal and biocidal addition of coastal power plants. Acknowledgements We thank Qi-Lang Xie, Xue-Liang Cai, and Jin-He Zheng etc. at Zhejiang Mariculture Research Institute for supports and facilities. We also thank Suzanne Bricker for the constructive comments. This work was supported by the Program on Research for Public Good of the Ministry of Science and Technology of the People’s Republic of China
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