Journal of Thermal Biology 26 (2001) 41–45
Temperature tolerance of some estuarine fishes S. Rajagurua,*, S. Ramachandranb a b
Centre of Advanced Study in Marine Biology, Parangipettai, Tamil Nadu 608502, India Institute for Ocean Management, Anna University, Chennai, Tamil Nadu 600025, India
Received 11 March 2000; received in revised form 29 April 2000; accepted 27 May 2000
Abstract The temperature tolerance of estuarine fishes Etroplus suratensis (Bloch), Therapon jarbua (Forsskal), Ambassis commersoni (Cuvier) collected from Vellar estuary, South India in 1986–87 were determined in the laboratory. E. suratensis and T. jarbua were found to be more tolerant to a wide range of temperature (16.5–41.58C for E. suratensis and 13.5–40.68C for T. jarbua), A. commersoni could tolerate from 15.5 to 38.58C. The tolerance area was found to be 512 units in E. suratensis, 629 units in T. jarbua and 442 units in A. commersoni. Among the fishes tested T. jarbua had a high tolerance area (629 units) than other fishes tested. It is evident from the results that 158C increase in acclimation temperature cause a shift of 4.028C (E. suratensis) and 3.058C (T. jarbua and A. commersoni) in upper incipient lethal temperature. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Estuarine fish; Tolerance; Resistance; Acclimation; Upper incipient lethal temperature (UILT); Lower incipient lethal temperature (LILT); Ultimate upper incipient lethal temperature; Biokinetic range; Trapezium polygon; Poikilotherms
1. Introduction Knowledge of tolerance limits of fishes to temperature is of ecological significance in assessing fish distribution, migration and their impact on ecosystems. The temperature tolerance and the rate of thermal acclimation of the estuarine fishes are studied to determine optimum and lethal levels of temperature. The thermal tolerance of various animal groups is reported in many scientific articles (Fry, 1947; Brett, 1956; Prosser, 1958; Kinne, 1970; Jobling, 1981; Satpathy et al., 1986; Willams, 1998 and Welch et al., 1998). Fry et al., (1942) and Brett, (1956) stated that the zone of thermal tolerance is bounded by two zones of thermal resistance in the cold and hot end of the biokinetic range. The lines that demarcate the zone of tolerance from the zones of resistance are the upper and lower incipient lethal temperatures (Fry et al., 1942). The incipient lethal level *Corresponding author. present address: Institute for Ocean Management, Anna University, Chennai 25 Tamilnadu, India. Fax: +91-44-2200158. E-mail addresses:
[email protected] (S. Rajaguru),
[email protected] (S. Ramachandran).
of temperature is defined as the temperature beyond which 50% of the population can no longer survive for an indefinite period of time (Fry et al., 1942). The incipient lethal level in the cold side of thermal tolerance is the lower incipient lethal level and the warmer end is known as the upper incipient lethal level (UILT). Fry et al. (1942) and Brett (1956) had also shown a shift in upper and lower incipient lethal levels due to changes in acclimation temperature as well as the incipient lethal levels are the same; beyond this, acclimation brings no change in incipient lethal temperatures. Thus, it could be derived that there is an ultimate upper incipient lethal temperature, which is the highest level to which the incipient lethal temperature can be raised by thermal acclimation. The present research work on estuarine fishes in tropical waters will be more useful for fish culturists and to those responsible for formulating regulation for thermal power plants.
2. Materials and methods The fishes Etroplus suratensis (Bloch), Therapon jarbua (Forsskal) and A. commersoni (Cuvier) were
0306-4565/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 3 0 6 - 4 5 6 5 ( 0 0 ) 0 0 0 2 4 - 3
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for these tolerance experiments. The number of fishes dead was recorded after 24 h of exposure. The percentage of animals that survived was plotted against the respective exposure temperatures in arithmetic graph. The temperature at which the 50% of the test animals may be expected to survive was predicted from the graph and that is known as incipient lethal level. At higher and lower lethal temperatures the incipient lethal levels are known as upper incipient lethal temperature and lower incipient lethal temperature, respectively. Following the method adopted for Carassius auratus (gold fish) (Fry et al., 1942), the upper and lower incipient lethal temperatures were plotted against acclimation temperature. Further construction of a diagonal line at an angle of 458 to the axes has provided a ready means of determining the ultimate upper lethal temperatures. The point to right where the to UILT reached 458 line and the point the to left where the lower incipient lethal temperature (LILT) reaches the 458 line mark the end of acclimation levels. Perpendicular lines were drawn from these points to the lethal lines. The two lethal lines together with the perpendicular lines from a polygon, gives the zones of tolerance. The enclosed area is the area of thermal tolerance and the value is expressed in centigrade scale as unit square degrees.
collected from the Vellar estuary and adjacent backwaters (Lat. 118290 N; Long. 798470 E) Tamil Nadu, S. India by cast net operation during the early morning and evening. Fish were maintained in fibreglass tanks (250–300 l capacity) containing filtered well-aerated estuarine water. The fishes were maintained at constant salinity 20% and temperature (28 18C). All fishes were acclimated in the laboratory for one week before being used for experiment. E. suratensis was fed with seaweed and T. jarbua and A. commersoni were fed with minced bivalve meat. They were starved for 24 h before the experiments started. The fishes were maintained above the ambient temperature in thermostatic water baths (50 l capacity) filled with filtered aerated estuarine water. A contacttype thermometer thermostat was used to maintain the temperature of the water bath with an accuracy of 0.18C at the desired levels above the ambient temperature. The water bath was aerated by means of compressed air passing through air stones and this maintains the oxygen tension at a constant level. The fishes weighing about 4–5 g were selected for the thermal tolerance experiments. They were acclimated at various constant temperatures viz., 20, 25, 28, 30 and 358C for a period of 7 days.
4. Results 3. Determination of lethal limits 4.1. Etroplus suratensis To determine lethal levels, the test animals are exposed for a particular period to various constant temperatures. For the present study, a 24 h test period was adopted to determine the LD 50 of lethal temperature. The test temperatures with an interval of 0.58C in high and lower temperature levels were taken
The upper and lower incipient lethal temperatures of E. suratensis determined in the series of constant acclimation temperatures viz., 20, 25, 28, 30 and 358C increased linearly with acclimation temperature (Table 1). The UILT and LILT for E. suratensis
Table 1 Upper and lower lethal temperature of Etroplus suratensis, Therapon jarbua and Ambasis commersoni Species
Acclimation temperature (8C)
UILT
LILT
E.suretensis
20 25 28 30 35
37.53 38.60 39.56 40.47 41.55
16.52 17.54 18.41 19.53 21.53
20 25 28 30 35
37.55 37.99 38.46 39.57 40.60
13.49 14.57 15.56 16.00 17.51
20 258 288 308 358
35.49 36.47 37.02 37.54 38.54
15.51 16.53 17.54 18.51 20.53
T. jarbua
A.commersoni
Regression equation UILT
Regression equation LILT
Y=31.862+0.278X r=0.9929
Y=9.344+0.339X r=0.982
Y=32.961+0.212X r=0.959
Y=7.976+0.269X r=0.997
Y=31.378+204X r=0.992
Y=8.353+0.339X r=0.985
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ultimate UILT and LILT predicted from the thermal tolerance polygon are 41.5 and 16.58C, respectively. The zone of thermal tolerance, which is enclosed within the polygon, formed by UILT and LILT expressed as units of tolerance (a unit of tolerance is equal to the area found by 18C and expressed as 8C2 (Brett,1956) for E. suratensis was about 512 units (Fig. 1a). 4.2. Therapon jarbua The UILT and LILT for T. jarbua obtained for constant temperature acclimation between 20 and 358C are presented in Table 1 and both the levels increased linearly with acclimation temperature (Fig. 1b). UILT for the fish acclimated at 208C was 37.68C and for the fish acclimated at 358C was 40.68C. LILT for the fish acclimated at 208C was 13.58C and for 358C acclimation was 17.58C. These results clearly show that a 158C increase in acclimation level brought about a shift of 3.058 in UILT and a shift of 4.028 in LILT. Thus, the rate of gain in heat resistance as a result of increasing the acclimation temperature was 0.203/8C rise in the acclimation temperature and the rate of gain in cold resistance was 0.268/8C decrease in the acclimation temperature. The ultimate UILT and LILT predicted from the thermal tolerance polygon were 40.6 and 13.58C, respectively. The total tolerance area predicted from the polygon was 629 units as shown in (Fig. 1b). 4.3. Ambasis commersoni Fig. 1.
acclimated at the above-mentioned temperatures increased linearly with acclimation temperature (Fig. 1a). This relation is described by regression equation Y=31.86+0.278X, where Y is lethal temperature (upper) X is the acclimation temperature, 0.278 is the slope or rate of increase with acclimation temperature and 31.86 is the Y-intercept at X equals zero (r=0.993). Likewise, the LILT is described by regression equation Y ¼ 9:34 þ 0:34X; where Y is the LILT and 0.34 is the slope or rate of increase with acclimation temperature and 9.34 is the Y-intercept at X equals Zero (r=0.982) UILT ranged from 37.5 to 41.58C and LILT ranged from 16.5 to 21.58C as acclimation temperature increased from 20 to 358C. It is evident from the results that a 158C increase in acclimation temperature caused a shift of 4.028C in UILT. The rate of gain of heat resistance as a result of increasing the acclimation temperature was 0.268/18C rise in the acclimation temperature and the rate of gain in cold resistance was 0.334/18C decrease in the acclimation temperature between 20 and 358C. The
The UILT and LILT determined for A. commersoni acclimated at various constant temperatures between 20 and 358C are presented in Table 1. It is evident from the results a 158C increase in acclimation temperature shifted UILT by 3.058C and LILT by 5.028C. The results further indicate that the rate of gain in heat resistance was 0.203/8C rise in acclimation temperature between 20 and 358C. The rate of gain of cold resistance was a fall of 0.334/ 8C decrease in acclimation temperature. The ultimate UILT and LILT from the thermal tolerance polygon were 38.5 and 15.58C, respectively. The tolerance area calculated from the polygon was 442 units (Fig 1c).
5. Discussion The upper and lower lethal temperature in aquatic poikilotherms depend upon the acclimation temperature. The most common phenomenon is Precht’s reasonable heat adaptation (Precht, 1967) and the results obtained in the present study show similar type of heat acclimation. UILT increased with increasing acclimation temperature from 20 to 358C, i.e., an
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increase in acclimation temperature caused a shift in UILT from 37.5 to 41.68C in E. suratensis; 37.6 to 40.68C in T. jarbua and 35.5 to 38.58C in A. commersoni. Similar observations have been made with trout Salvelinus fontinalis (Fry et al., 1946), salmoniid species (Brett, 1944, 1956), the marine species (Hoff and Westman, 1966), Salmo gairdneri (Bidgood, 1980), Rhinomugil corsula (Kutty et al., 1980) and Chalcalburnus chalcoides (Al-Habbib, 1981). The rate of gain of heat resistance or acclimation response ratio (ARR) as a result of increasing the acclimation temperature was about 0.268/8C in E. suratensis, 0.203/8C in T. jarbua and A. commersoni. The rate of gain of cold resistance or ARR value as a result of increasing the acclimation temperature was about 0.334/8C in E. suratensis and A. commersoni and 0.268/8C in T. jarbua. This ARR is high as compared with other fish species reported except gold fish (Fry, 1942). In gold fish, the rate of gain of heat resistance was 1/38C rise in acclimation temperature. In S. fontinalis a 78C increase in acclimation temperature caused an increase in the thermal resistance by 18C (Fry et al., 1946) and in Chalcalburnus chalcoides (Al-Habbib, 1981) the rate of heat resistance gain was about 1/108C increase in acclimation temperature. The results of the effect of acclimation temperature on lower lethal temperature in three species, E. suratensis, T. jarbua and A. commersoni indicate that the fishes acclimated at high temperatures had higher low lethal temperatures than those acclimated to low temperatures. This is according to Precht’s reasonable heat adaptation and this is shown in many cold-blooded animals (Precht et al., 1973). The rate of gain of cold resistance was 2/ 58C decrease in acclimation temperature between 35 and 308C in E. suratensis, 1.5/58C in T. jarbua and 2/58C in A. commersoni, whereas the rate of gain of cold resistance was 1.5/58C decrease in the acclimation temperature between 30 and 208C in E. suratensis and 1/48C in T. jarbua and 1.5/58C in A. commersoni. A similar decrease in the acclimation temperature caused an increase in the cold resistance in G. migricans (Doudoroff, 1942), four cyprinid species (Fry et al, 1942), five salmoniid species (Brett, 1952), Rhinomugil corsula (Kutty et al.,1980) and Chalcalburnus chalcoides (Al-Habbib, 1981). The overall relation between the acclimation temperature and lethal temperature is represented by the trapezium polygon for the three species shown in Fig. 1a–c. Among the fishes tested T. jarbua had a higher tolerance area (629 units) than E. suratensis (512 units) and A. commersoni (442 units). The value of E. suratensis and A. commersoni are similar to those reported for five fresh water salmoniid species ranged from 450 to 529 units (Brett, 1952). The tolerance area of T. jarbua is similar to those obtained for Salvelinus
fontinalis, i.e. 625 units (Fry et al., 1946). However these values are less than those reported for cyprinidae (740–940 units) and ameiuridae species (970–1162 units) (Hart, 1947). Similarly, the thermal tolerance zone of 541, 625 and 640 units were found in C. artedii (Edsall and Colby, 1970), Onchorynchus (Fry et al., 1946), Chalcaburnus chalcoides (Al-Habbib, 1981), respectively. Among the few tropical species subjected to the study of thermal responses (Allanson and Noble, 1964; Ananthakrishnan and Srinivasan, 1977; Kutty et al., 1980) the complete thermal tolerance has not been calculated except for Ophiocephalus punctatus by Ananthakrishnan and Kutty (1976), which has a tolerance area of 410 units. It is clear from the results that the fishes T. jarbua and A. commersoni showed an increasing acclimation towards lower than higher temperatures, where as the fish E. suratensis showed an increasing acclimation towards higher than lower temperature. In addition, the difference in the median environmental temperature (288C) and the ultimate UILT is 12.68C for T. jarbua, 10.58C for A. commersoni and 13.58C for E . suratensis, but the difference with ultimate LILT is 14.58C for T. jarbua, 12.58C for A. commersoni and 11.58C for E. suratensis. These results strongly suggest the preference of fishes towards lower than higher temperatures except E. suratensis which has preference towards higher temperatures. It is also interesting to note that the fishes are unable to sustain very low temperatures below 16.58C (E. suratensis) 13.58C (T. jarbua) and 15.58C (A. commersoni) for a prolonged period. While many arctic animals are able to live below the freezing temperature (Prosser, 1958). This suggests that the mechanism of break down at lower temperatures in the topical animals is probably different from arctic and temperate animals (Paulpandian, 1967). There has been increasing interest in the possible use of thermal effluent to promote fish growth (Sylvester, 1975; Aston et al., 1976) and there are commercial and pilot-scale farms using power station cooling water. Holt and Strawn (1976) suggested that the accurate information concerning the optimum temperatures for growth and temperature tolerance ranged would lead to the selection of more suitable species. Among the major problems faced by culturists of red sea bream, Chrysophyrs major, in Japan are reduced growth and increased mortality during the summer months (Kitazima, 1969), during which the sea surface temperature exceeds 308C and this approaching the ultimate upper incipient lethal temperature (328C) of the species (Woo and Fund, 1980). Therefore, data on the temperature tolerance of the cultivable species should be considered when selection of species and assessing the suitability of sites for culture.
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Acknowledgements The first author wishes to thank the late Prof. A.L. Paulpandian for sincere guidance and the Director, Centre of Advanced Study in Marine Biology, Annamalai University, Parangipettai, India, for providing facilities and the University Grants Commission for financial assistance.
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