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Respiration rate of the kuruma prawn, Penaeus japonicus Bate, is not increased by handling at low temperature (12°C)
Aquaculture, 114 (1993) 229-235 Elsevier Science Publishers B.V., Amsterdam
229
AQUA 4007 I
Respiration rate of the kuruma prawn, Penaeus japonicus Bate, is not increased by handling at low temperature ( 12 OC) Brian D. Paterson International Food Institute of Queensland, Queensland Department ofPrimary Industries, Hamilton, Qld., Australia (Accepted
10 March 1993)
ABSTRACT Kuruma prawns (Penaeus japonicus) are immobilised by cooling and then handled individually when packed for live shipment out of water. An automatic respirometer, with modifications to improve water circulation, was used to measure the respiration rate of settled and handled adult P. japonicus at 12, 17 and 22°C. Handling increased the respiration rate of the prawns at the two highest temperatures but had no effect at 12 oC. Thus, the contribution that handling normally made to metabolic rate was removed when the prawns were cold “anaesthetised”.
INTRODUCTION
The kuruma prawn, Penaeus japonicus Bate, is shipped live to markets in Japan and the quantity of live prawns imported into that country over the last 4 years has increased dramatically. Recent interest in exporting this prawn from Australia to Japan has prompted research into techniques of handling live penaeid prawns, particularly P. japonicus. Before export, kuruma prawns are cooled to a point at which they are unable to right themselves ( lo- 14 "C) , then taken from the water and packed into chilled dry sawdust (Shigeno, 1979). The prawns are handled individually, a labour-intensive process, to check for any weakness or injury that could compromise their survival. It is a general principle that handling increases the respiration rate of crustacea (Winkler, 1987), apparently by increasing the activity of the animals (e.g. walking or swimming). For this reason, some crustaceans are vulnerable to disturbance during live transport in air (Taylor and Whiteley, 1989). If activity is the major response of the prawn Correspondence to: B.D. Paterson, International Food Institute of Queensland, Queensland partment of Primary Industries, 19 Hercules St, Hamilton, Queensland, Australia 4007.
0044-8486/93/$06.00
0 1993 Elsevier Science Publishers
B.V. All rights reserved.
De-
230
B.D. PATERSON
to handling, it follows that if it can be anaesthetised (by reducing the temperature), the effect of handling on respiration rate should be removed altogether. This paper considers the effect of handling at different temperatures on the respiration rate of the kuruma prawn. METHODS AND MATERIALS
The P. jupo@cus used in these experiments were grown at Moreton Bay Prawn Farm, near Brisbane, on the southern coast of Queensland, Australia. Prawns of either sex (ranging in weight from 8 to 25 g and moult stage C-D1 (Smith and Dall, 1985 ) ) were used. Prawns were harvested and kept for at least a week in a 1000 1 recirculating seawater aquarium (22°C) lined with sand (5 cm deep) prior to experiments. Experiments were carried out in a second aquarium (salinity 35 ppt, 22°C) without a sand bed. These tanks were located in an air-conditioned room. The water in the sand tank was circulated through a biological filter and changed periodically using water from the intake pond of the prawn farm. The salinity of the sand tank was kept between 30 ppt and 35 ppt. The temperature of both tanks was controlled to within 0.1 “C using process controllers by circulating the water through a plastic heat exchanger immersed in an ice slurry.
Oxygen uptake rate was measured using an automatic respirometer similar to that used by Dal1 ( 1986) for studies of respiration of the brown tiger prawn, P. esculentus Haswell. The volume of the chamber ( 800 ml) was smaller than that used by Dal1 ( 1986) (i.e. > 1000 ml). The chamber was made from an acrylic canister (diameter 6 cm, length 27 cm) (Fig. 1). The low volume reduced the amount of dissolved oxygen available, which magnified the impact of the prawn’s consumption (particularly important at low temperature) when the chamber was closed for short periods. The narrow design did not compromise mixing of the chamber contents. The canister normally remained submerged in one of the aquariums, allowing animals to be transferred between chamber and aquarium without removing the chamber or the animal from the water. Water was pumped into and out of the chamber using a submersible aquarium pump and plastic tubing ( 3 mm i.d.). The flow of water through the intake tube was controlled by a 240 V AC solenoid valve that was operated either manually or by a 60 min power timer. The power timer allowed the respirometer to cycle continually between “closed” and “open” during experimental treatments (e.g. cooling). The oxygen tension in the respiration chamber was monitored using an O2 sensor and meter connected to a portable chart recorder.
RESPI~TION
floor
RATE OF PENAEUS ~~P~~~Cff~
stirrer
231
oxygen sensor
Fig. 1. Cylindrical respirometer chamber. The screw-top lid of the canister was made watertight by using a rubber washer, and the oxygen sensor was inserted through a 15 mm aperture in the lid and sealed with “0” rings. Water movement at the sensor membrane was maintained using a stirring bar, which, in conjunction with the incomplete floor inside the canister, also circulated water through the rest of the canister. A gauze screen, glued to a cylindrical insert, separated the animal from the stirring bar and oxygen sensor. Water entered through a 2 mm tap at the far end of the canister and exited from a similar tap closer to the oxygen sensor. Any exchange of water between the canister and these taps during the closed stage was negligible.
Experimental design During storage in the sand tank, the prawns were fed daily with commercial prawn food ( Charoen Pokaphand, Thail~d ) and supplemented with chopped prawn, squid and scallop waste, as available. The food pellets were dispensed in the late afternoon through an automatic feeder. Uneaten food was removed the following morning. The prawns were allowed to acclimate without feed to the ambient conditions in the expe~mental tank for at least 2 days prior to measuring oxygen uptake rate. Photoperiod was controlled by a time switch ( 12 h on/ 12 h off) and a gradual transition from light to dark was adopted to avoid startling the prawns. These experiments were time consuming, and required several months (from October 1990 to May 199 1) to collect data from many animals. During this time, the prawns were growing and seasonal changes in pond temperature occurred, Experiments in which prawns were cooled to the inte~e~ate temperature of 17 oC were begun in February, so the range of body size used in this treatment was narrower ( 15 to 25 g) than in the others (9 to 25 g). It was therefore necessary to consider body size of the prawns as a variable in the subsequent analysis. Average weekly pond temperature was about 3 1 “C in summer and fell to about 15 ‘C in winter during these experiments, and respiration experiments, at 22 ‘C, 17 oC and 12 ’ C, were repeated throughout this period, to average out any seasonal effects. Effect of temperature’and handling on respiration rate Records were taken of oxygen tension in the closed chamber either for 30 min immediately after a prawn was placed into the chamber (“handled”)
B.D. PATERSON
232
from the aquarium, or for 30 min after the prawn had been allowed to recover from handling (“settled”). The “settled” prawns were left overnight in the canister (with the respirometer continually alternating between closed and open mode) before recording oxygen uptake rate. Measurements of settled and handled prawns were made at 22 ‘C or after cooling the prawns at a rate of 3 “C h- ’ to either 17 0C or 12 *C. Cooling experiments were conducted throughout the 8 month study, so that trials at a given temperature were conducted regardless of season. Respiration rate was calculated after correcting for changes in oxygen tension in the empty chamber. Two replicates of this experiment were completed in a week, subject to the availability of intermoult prawns. Statistics Weight-specific respiration rate (respiration per gram of body weight ) is known to be correlated with prawn weight and, as circumstances prevented prawns of similar size being used for each trial, the absolute respiration rate data (,umol O2 min- ’ ) for the two handling treatments and the three temperatures were subjected to analysis of covariance (ANCOVA) using prawn weight as the covariate. A separate multiple regression analysis was used to describe the relationship between body size and respiration rate at the three temperatures. RESULTS
The settled or handled weight-specific respiration rate of intermoult P. japonicus at various temperatures is shown in Table 1. Handling raised the respiration rate of all except those prawns at 12”C, though the wide variation seen in some treatments creates faculty in inte~retation (pa~icularly at 17°C). The wide variation in respiration rate of handled prawns at 22°C shows that the data do not conform to a normal distribution. TABLE 1 Effect of handling temperatures Treatment (“C)
22 17 12
on the mean respiration
Respiration
rate of the kurtnna prawn P. jtzponicus at different
rate’ (firno O2 kg-’ min-‘)
Settled
Handled
79.1k31.1 (19)2 28.257.8 (13) 22.328.4 (13)
131.7+5s.5 (22) 47.3+ 19.6 (13) 21.6f9.1 (13)
‘Raw data ( ?I s.d.) prior to adjustment 2Number of prawns.
for body sizei
RESPIRATION RATE OF PENAEUS
JAPONICUS
233
Some of the variation of the data from settled prawns was accounted for by body size. The ANCOVA of absolute respiration rate (corrected to a body size of 15.3 g) showed a highly significant effect of both temperature and handling upon respiration, but, in addition, there was a highly significant interaction between temperature and handling (P< 0.0 1) . Handling the prawns at 12 ’ C had no effect on their respiration rate, whereas the same treatment at higher temperature produced a significant rise in respiration rate that became more pronounced at the highest temperature (PC 0.05 at 17 “C, PC 0.0 1 at 22°C). DISCUSSION
One of the major ways that handling affects the respiration rate of animals is by increasing their locomotor activity. In both P. japonicus and P. emdentus, respiration rate changes with the activity state of the prawn (Truchot and Jouve-Duhamel, 1983; Dall, 1986), and in this study the respiration rate of prawns disturbed at 22°C reflected activity ranging from excited swimming to “playing possum” (P. japo~~~s will sometimes curl up on its side on the tank bottom rather than flee from disturbance). Therefore, preventing activity is an obvious way to reduce the metabolic stress experienced by crustaceans during live handling and transport. Chemical anaesthetics are sometimes used to reduce metabolic rate when transporting live fish (Collins, 1990), but this practice is discouraged when the product is destined for human consumption. However, cooling is a well understood means of reducing the metabolic rate of crustaceans during commercial transport both in and out of water. As falling temperature will increasingly incapacitate the prawn, it follows that the contribution of activity to respiration rate will also decline. For example, Van Donk and De Wilde ( 1981) found that the shrimp Crangon crangon showed a narrowing of its “scope for activity” (the difference between active and inactive respiration rate) as the temperature fell. Several interacting factors probably lowered the respiration rate of P. japonicus in the cold. A reduction in metabolic rate is expected from the decrease in temperature alone, but oxygen uptake can itself be interrupted at low temperature by the failure of the oxygen transport pigment in the blood to release its oxygen in the cold (Mauro and Mangum, 1982). Added to these physiological effects, at low temperature nerve and muscle function in crustaceans becomes physically blocked (Blundon, 1989). Penaeids often respond to a drop in temperature below a certain level by burying in sand and remaining there (Hill, 1985 ) . At extremely low temperatures, (e.g., < 12 *C ) the prawns are probably so torpid that they are physically unable to emerge from the sand. Prawns that fail to bury under these conditions soon fall over and come to lie unprotected on the sediment surface
234
B.D. PATERSON
(Aldrich et al., 1968 ). P. japo~i~~sthat are cooled commercially for live export experience a period of reflexive jumping and then fall over. They are no longer able to stand upright at temperatures below about 13 ‘C. However, this response is probably subject to seasonal acclimatisation of the nervous system (Blundon, 1989). Comparing the respiration data obtained in this study to those of previous workers hi~li~ts possible differences between species of prawns. The mean respiration rate of settled P. japonicus at 22°C was higher than the standard respiration rate of P. esculentus at 20 oC (i.e., 22 pm01 O2 kg- ’ min- ’ ) (Dall, 1986). The prawns studied here were not totally inactive in the respirometer, even though it was daylight. Therefore, the daylight shut-down of metabolism may be more pronounced in the latter species. Inactive P. es~~e~t~s cooled to 15°C have a lower respiration rate (Dal& 1986) than that of P. japo~ic~s at 12”C, a temperature at which the contribution of activity to respiration rate is expected to be minimised. This probably occurs because P. esculentus is less tolerant of low temperatures than P. japonicus. Differences exist in published values of the respiration rate of the black tiger prawn, P. ~0~0~0~. Kurmaly et al. ( 1989) report a respiration rate of 55 pm01 O2 kg-’ min-’ at 15°C and Liao and Murai ( 1986) found a rate of 59 pm01 O2 kg- ’ min- * at 20°C. Therefore, differences between results obtained from other species may reflect differences in the circumstances of the experiment. Laboratory artefacts possibly prevented the kuruma prawns in this study from showing a respiration rate typical of a buried prawn, in the laboratory, during daylight. European lobster, Homarus gammarus, increases its respiration rate in response to handling in air (Taylor and Whiteley, 1989; Whiteley et al., 1990). This indicates that the lobsters may not be cooled sufficiently to remove the effect of handling on activity. In practice, temperatures that anaesthetise crustaceans are necessary only when transposing crustaceans for long periods out of water ( l-3 days for P. japonicus) since crustaceans only need to be cooled enough to get them to market alive. So, when packing live prawns for export, there is no evidence that handling them in water at low temperature (i.e. 12’ C) causes any increase in respiration rate and, by implication, in metabolic rate. Thus, no special precautions are required to minimise handling stress when the prawns are first packed. The benefit of cooling the prawns does not appear to be due to the effect of “acclimation” to the cold, but rather to a physiological shock that allows them to be handled more conveniently.
Thanks to the project leader B. Goodrick and to S. Grauf of IFIQ for helping to maintain the holding tanks. Stephen Nottingham (IFIQ ) provided sta-
RESPIRATION RATE OF PENAEUS JAPONKUS
235
tistical support. The staff of Moreton Bay Prawn Farm kindly accommodated our laboratory for the duration of the study. Fisheries Branch (QDPI) and the crew of the FRV Gwendolyn May are thanked for collecting the P. japonicus broodstock. This research was carried out during a study of live prawn handling supported by the Fishing Industry Research and Development Trust Account (FIRDTA). REFERENCES Aldrich, D.V., Wood, C.E. and Baxter, K.N., 1968. An ecological interpretation of low temperature responses in Penaeus aztecus and Penaeus setiferus postlarvae. Bull. Mar. Sci., 18: 6 l71. Blundon, J.A., 1989. Effects of temperature and thermal history on neuromuscular properties of two crustacean species. J. Comp. Physiol. B, 158: 689-696. Collins, C., 1990. Live-hauling warm water fish. Aquaculture Magazine, July/August: 70-76. Dall, W., 1986. Estimation of routine metabolic rate in a penaeid prawn, Penaeus esczdentus Haswell. J. Exp. Mar. Biol. Ecol., 96: 57-74. Hill, B.J., 1985. Effect of temperature on duration of emergence, speed of movement, and catchability ofthe prawn Penaeus esculentus. In: P.C. Rothlisberg, B.J. Hill and D.J. Staples (Editors), Second Aust. Natl. Prawn Sem., 22-26 October 1984, NPS2, Cleveland, Australia, pp. 77-83. Kurmaly, IS., Yule, A.B. and Jones, D.A., 1989. Effects of body size and temperature on the metabolic rate of Penaeus monodun. Mar. Biol., 103: 25-30. Liao, I-C. and Murai, T., 1986. Effects of dissolved oxygen, temperature and salinity on the dissolved oxygen consumption of the grass shrimp, Penaeus monodon. In: J.L. Maclean, L.B. Dizon and L.V. Hosillos (Editors), The First Asian Fisheries Forum. Asian Fisheries Society, Manila, Philippines, pp. 641-646. Mauro, N.A. and Mangum, C.P., 1982. The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. I. Interspecific responses to seasonal differences in temperature. J. Exp. Zool., 219: 179-188. Shigeno, K., 1979. Problems in Prawn Culture. Aquaculture Series 19. Balkema Press, Rotterdam, Netherlands, 103 pp. Smith, D.M. and Dall, W., 1985. Moult staging the tiger prawn Penaeus esculentus. In: P.C. Rothlisberg, B.J. Hill and D.J. Staples (Editors), Second Aust. Natl. Prawn Sem., 22-26 October 1984, NPS2, Cleveland, Australia, pp. 85-93. Taylor, E.W. and Whiteley, N.M., 1989. Oxygen transport and acid-base balance in the haemolymph of the lobster, Homarus gammarus, during aerial exposure and re-submersion. J. Exp. Biol., 144: 4 17-436. Truchot, J.P. and Jouve-Duhamel, A., 1983. Consommation d’oxygene de la crevette japonaise, Penaeusjaponicus, en fonction de l’oxygenation du milieu: effets de la temperature et de l’acclimatation a des conditions ambiantes hypoxiques. Bases biologiques de l’aquaculture. Montpellier, IFREMER Actes de Colloques, 1: 245-254. Van Donk, E. and De Wilde, P.A.W.J., 198 1. Oxygen consumption and motile activity of the brown shrimp Crangon crangun related to temperature and body size. Neth. J. Sea Res., 15: 54-64. Whiteley, N.M., Al-Wassia, A.H. and Taylor, E.W., 1990. The effect of temperature, aerial exposure and disturbance on oxygen consumption in the lobster, Homarus gammarus (L. ). Mar. Behav. Physiol., 17: 213-222. Winkler, P., 1987. Effects of handling on the in situ oxygen consumption of the American lobster (Homarus americanus). Comp. Biochem. Physiol., 87A: 69-7 1.
229
AQUA 4007 I
Respiration rate of the kuruma prawn, Penaeus japonicus Bate, is not increased by handling at low temperature ( 12 OC) Brian D. Paterson International Food Institute of Queensland, Queensland Department ofPrimary Industries, Hamilton, Qld., Australia (Accepted
10 March 1993)
ABSTRACT Kuruma prawns (Penaeus japonicus) are immobilised by cooling and then handled individually when packed for live shipment out of water. An automatic respirometer, with modifications to improve water circulation, was used to measure the respiration rate of settled and handled adult P. japonicus at 12, 17 and 22°C. Handling increased the respiration rate of the prawns at the two highest temperatures but had no effect at 12 oC. Thus, the contribution that handling normally made to metabolic rate was removed when the prawns were cold “anaesthetised”.
INTRODUCTION
The kuruma prawn, Penaeus japonicus Bate, is shipped live to markets in Japan and the quantity of live prawns imported into that country over the last 4 years has increased dramatically. Recent interest in exporting this prawn from Australia to Japan has prompted research into techniques of handling live penaeid prawns, particularly P. japonicus. Before export, kuruma prawns are cooled to a point at which they are unable to right themselves ( lo- 14 "C) , then taken from the water and packed into chilled dry sawdust (Shigeno, 1979). The prawns are handled individually, a labour-intensive process, to check for any weakness or injury that could compromise their survival. It is a general principle that handling increases the respiration rate of crustacea (Winkler, 1987), apparently by increasing the activity of the animals (e.g. walking or swimming). For this reason, some crustaceans are vulnerable to disturbance during live transport in air (Taylor and Whiteley, 1989). If activity is the major response of the prawn Correspondence to: B.D. Paterson, International Food Institute of Queensland, Queensland partment of Primary Industries, 19 Hercules St, Hamilton, Queensland, Australia 4007.
0044-8486/93/$06.00
0 1993 Elsevier Science Publishers
B.V. All rights reserved.
De-
230
B.D. PATERSON
to handling, it follows that if it can be anaesthetised (by reducing the temperature), the effect of handling on respiration rate should be removed altogether. This paper considers the effect of handling at different temperatures on the respiration rate of the kuruma prawn. METHODS AND MATERIALS
The P. jupo@cus used in these experiments were grown at Moreton Bay Prawn Farm, near Brisbane, on the southern coast of Queensland, Australia. Prawns of either sex (ranging in weight from 8 to 25 g and moult stage C-D1 (Smith and Dall, 1985 ) ) were used. Prawns were harvested and kept for at least a week in a 1000 1 recirculating seawater aquarium (22°C) lined with sand (5 cm deep) prior to experiments. Experiments were carried out in a second aquarium (salinity 35 ppt, 22°C) without a sand bed. These tanks were located in an air-conditioned room. The water in the sand tank was circulated through a biological filter and changed periodically using water from the intake pond of the prawn farm. The salinity of the sand tank was kept between 30 ppt and 35 ppt. The temperature of both tanks was controlled to within 0.1 “C using process controllers by circulating the water through a plastic heat exchanger immersed in an ice slurry.
Oxygen uptake rate was measured using an automatic respirometer similar to that used by Dal1 ( 1986) for studies of respiration of the brown tiger prawn, P. esculentus Haswell. The volume of the chamber ( 800 ml) was smaller than that used by Dal1 ( 1986) (i.e. > 1000 ml). The chamber was made from an acrylic canister (diameter 6 cm, length 27 cm) (Fig. 1). The low volume reduced the amount of dissolved oxygen available, which magnified the impact of the prawn’s consumption (particularly important at low temperature) when the chamber was closed for short periods. The narrow design did not compromise mixing of the chamber contents. The canister normally remained submerged in one of the aquariums, allowing animals to be transferred between chamber and aquarium without removing the chamber or the animal from the water. Water was pumped into and out of the chamber using a submersible aquarium pump and plastic tubing ( 3 mm i.d.). The flow of water through the intake tube was controlled by a 240 V AC solenoid valve that was operated either manually or by a 60 min power timer. The power timer allowed the respirometer to cycle continually between “closed” and “open” during experimental treatments (e.g. cooling). The oxygen tension in the respiration chamber was monitored using an O2 sensor and meter connected to a portable chart recorder.
RESPI~TION
floor
RATE OF PENAEUS ~~P~~~Cff~
stirrer
231
oxygen sensor
Fig. 1. Cylindrical respirometer chamber. The screw-top lid of the canister was made watertight by using a rubber washer, and the oxygen sensor was inserted through a 15 mm aperture in the lid and sealed with “0” rings. Water movement at the sensor membrane was maintained using a stirring bar, which, in conjunction with the incomplete floor inside the canister, also circulated water through the rest of the canister. A gauze screen, glued to a cylindrical insert, separated the animal from the stirring bar and oxygen sensor. Water entered through a 2 mm tap at the far end of the canister and exited from a similar tap closer to the oxygen sensor. Any exchange of water between the canister and these taps during the closed stage was negligible.
Experimental design During storage in the sand tank, the prawns were fed daily with commercial prawn food ( Charoen Pokaphand, Thail~d ) and supplemented with chopped prawn, squid and scallop waste, as available. The food pellets were dispensed in the late afternoon through an automatic feeder. Uneaten food was removed the following morning. The prawns were allowed to acclimate without feed to the ambient conditions in the expe~mental tank for at least 2 days prior to measuring oxygen uptake rate. Photoperiod was controlled by a time switch ( 12 h on/ 12 h off) and a gradual transition from light to dark was adopted to avoid startling the prawns. These experiments were time consuming, and required several months (from October 1990 to May 199 1) to collect data from many animals. During this time, the prawns were growing and seasonal changes in pond temperature occurred, Experiments in which prawns were cooled to the inte~e~ate temperature of 17 oC were begun in February, so the range of body size used in this treatment was narrower ( 15 to 25 g) than in the others (9 to 25 g). It was therefore necessary to consider body size of the prawns as a variable in the subsequent analysis. Average weekly pond temperature was about 3 1 “C in summer and fell to about 15 ‘C in winter during these experiments, and respiration experiments, at 22 ‘C, 17 oC and 12 ’ C, were repeated throughout this period, to average out any seasonal effects. Effect of temperature’and handling on respiration rate Records were taken of oxygen tension in the closed chamber either for 30 min immediately after a prawn was placed into the chamber (“handled”)
B.D. PATERSON
232
from the aquarium, or for 30 min after the prawn had been allowed to recover from handling (“settled”). The “settled” prawns were left overnight in the canister (with the respirometer continually alternating between closed and open mode) before recording oxygen uptake rate. Measurements of settled and handled prawns were made at 22 ‘C or after cooling the prawns at a rate of 3 “C h- ’ to either 17 0C or 12 *C. Cooling experiments were conducted throughout the 8 month study, so that trials at a given temperature were conducted regardless of season. Respiration rate was calculated after correcting for changes in oxygen tension in the empty chamber. Two replicates of this experiment were completed in a week, subject to the availability of intermoult prawns. Statistics Weight-specific respiration rate (respiration per gram of body weight ) is known to be correlated with prawn weight and, as circumstances prevented prawns of similar size being used for each trial, the absolute respiration rate data (,umol O2 min- ’ ) for the two handling treatments and the three temperatures were subjected to analysis of covariance (ANCOVA) using prawn weight as the covariate. A separate multiple regression analysis was used to describe the relationship between body size and respiration rate at the three temperatures. RESULTS
The settled or handled weight-specific respiration rate of intermoult P. japonicus at various temperatures is shown in Table 1. Handling raised the respiration rate of all except those prawns at 12”C, though the wide variation seen in some treatments creates faculty in inte~retation (pa~icularly at 17°C). The wide variation in respiration rate of handled prawns at 22°C shows that the data do not conform to a normal distribution. TABLE 1 Effect of handling temperatures Treatment (“C)
22 17 12
on the mean respiration
Respiration
rate of the kurtnna prawn P. jtzponicus at different
rate’ (firno O2 kg-’ min-‘)
Settled
Handled
79.1k31.1 (19)2 28.257.8 (13) 22.328.4 (13)
131.7+5s.5 (22) 47.3+ 19.6 (13) 21.6f9.1 (13)
‘Raw data ( ?I s.d.) prior to adjustment 2Number of prawns.
for body sizei
RESPIRATION RATE OF PENAEUS
JAPONICUS
233
Some of the variation of the data from settled prawns was accounted for by body size. The ANCOVA of absolute respiration rate (corrected to a body size of 15.3 g) showed a highly significant effect of both temperature and handling upon respiration, but, in addition, there was a highly significant interaction between temperature and handling (P< 0.0 1) . Handling the prawns at 12 ’ C had no effect on their respiration rate, whereas the same treatment at higher temperature produced a significant rise in respiration rate that became more pronounced at the highest temperature (PC 0.05 at 17 “C, PC 0.0 1 at 22°C). DISCUSSION
One of the major ways that handling affects the respiration rate of animals is by increasing their locomotor activity. In both P. japonicus and P. emdentus, respiration rate changes with the activity state of the prawn (Truchot and Jouve-Duhamel, 1983; Dall, 1986), and in this study the respiration rate of prawns disturbed at 22°C reflected activity ranging from excited swimming to “playing possum” (P. japo~~~s will sometimes curl up on its side on the tank bottom rather than flee from disturbance). Therefore, preventing activity is an obvious way to reduce the metabolic stress experienced by crustaceans during live handling and transport. Chemical anaesthetics are sometimes used to reduce metabolic rate when transporting live fish (Collins, 1990), but this practice is discouraged when the product is destined for human consumption. However, cooling is a well understood means of reducing the metabolic rate of crustaceans during commercial transport both in and out of water. As falling temperature will increasingly incapacitate the prawn, it follows that the contribution of activity to respiration rate will also decline. For example, Van Donk and De Wilde ( 1981) found that the shrimp Crangon crangon showed a narrowing of its “scope for activity” (the difference between active and inactive respiration rate) as the temperature fell. Several interacting factors probably lowered the respiration rate of P. japonicus in the cold. A reduction in metabolic rate is expected from the decrease in temperature alone, but oxygen uptake can itself be interrupted at low temperature by the failure of the oxygen transport pigment in the blood to release its oxygen in the cold (Mauro and Mangum, 1982). Added to these physiological effects, at low temperature nerve and muscle function in crustaceans becomes physically blocked (Blundon, 1989). Penaeids often respond to a drop in temperature below a certain level by burying in sand and remaining there (Hill, 1985 ) . At extremely low temperatures, (e.g., < 12 *C ) the prawns are probably so torpid that they are physically unable to emerge from the sand. Prawns that fail to bury under these conditions soon fall over and come to lie unprotected on the sediment surface
234
B.D. PATERSON
(Aldrich et al., 1968 ). P. japo~i~~sthat are cooled commercially for live export experience a period of reflexive jumping and then fall over. They are no longer able to stand upright at temperatures below about 13 ‘C. However, this response is probably subject to seasonal acclimatisation of the nervous system (Blundon, 1989). Comparing the respiration data obtained in this study to those of previous workers hi~li~ts possible differences between species of prawns. The mean respiration rate of settled P. japonicus at 22°C was higher than the standard respiration rate of P. esculentus at 20 oC (i.e., 22 pm01 O2 kg- ’ min- ’ ) (Dall, 1986). The prawns studied here were not totally inactive in the respirometer, even though it was daylight. Therefore, the daylight shut-down of metabolism may be more pronounced in the latter species. Inactive P. es~~e~t~s cooled to 15°C have a lower respiration rate (Dal& 1986) than that of P. japo~ic~s at 12”C, a temperature at which the contribution of activity to respiration rate is expected to be minimised. This probably occurs because P. esculentus is less tolerant of low temperatures than P. japonicus. Differences exist in published values of the respiration rate of the black tiger prawn, P. ~0~0~0~. Kurmaly et al. ( 1989) report a respiration rate of 55 pm01 O2 kg-’ min-’ at 15°C and Liao and Murai ( 1986) found a rate of 59 pm01 O2 kg- ’ min- * at 20°C. Therefore, differences between results obtained from other species may reflect differences in the circumstances of the experiment. Laboratory artefacts possibly prevented the kuruma prawns in this study from showing a respiration rate typical of a buried prawn, in the laboratory, during daylight. European lobster, Homarus gammarus, increases its respiration rate in response to handling in air (Taylor and Whiteley, 1989; Whiteley et al., 1990). This indicates that the lobsters may not be cooled sufficiently to remove the effect of handling on activity. In practice, temperatures that anaesthetise crustaceans are necessary only when transposing crustaceans for long periods out of water ( l-3 days for P. japonicus) since crustaceans only need to be cooled enough to get them to market alive. So, when packing live prawns for export, there is no evidence that handling them in water at low temperature (i.e. 12’ C) causes any increase in respiration rate and, by implication, in metabolic rate. Thus, no special precautions are required to minimise handling stress when the prawns are first packed. The benefit of cooling the prawns does not appear to be due to the effect of “acclimation” to the cold, but rather to a physiological shock that allows them to be handled more conveniently.
Thanks to the project leader B. Goodrick and to S. Grauf of IFIQ for helping to maintain the holding tanks. Stephen Nottingham (IFIQ ) provided sta-
RESPIRATION RATE OF PENAEUS JAPONKUS
235
tistical support. The staff of Moreton Bay Prawn Farm kindly accommodated our laboratory for the duration of the study. Fisheries Branch (QDPI) and the crew of the FRV Gwendolyn May are thanked for collecting the P. japonicus broodstock. This research was carried out during a study of live prawn handling supported by the Fishing Industry Research and Development Trust Account (FIRDTA). REFERENCES Aldrich, D.V., Wood, C.E. and Baxter, K.N., 1968. An ecological interpretation of low temperature responses in Penaeus aztecus and Penaeus setiferus postlarvae. Bull. Mar. Sci., 18: 6 l71. Blundon, J.A., 1989. Effects of temperature and thermal history on neuromuscular properties of two crustacean species. J. Comp. Physiol. B, 158: 689-696. Collins, C., 1990. Live-hauling warm water fish. Aquaculture Magazine, July/August: 70-76. Dall, W., 1986. Estimation of routine metabolic rate in a penaeid prawn, Penaeus esczdentus Haswell. J. Exp. Mar. Biol. Ecol., 96: 57-74. Hill, B.J., 1985. Effect of temperature on duration of emergence, speed of movement, and catchability ofthe prawn Penaeus esculentus. In: P.C. Rothlisberg, B.J. Hill and D.J. Staples (Editors), Second Aust. Natl. Prawn Sem., 22-26 October 1984, NPS2, Cleveland, Australia, pp. 77-83. Kurmaly, IS., Yule, A.B. and Jones, D.A., 1989. Effects of body size and temperature on the metabolic rate of Penaeus monodun. Mar. Biol., 103: 25-30. Liao, I-C. and Murai, T., 1986. Effects of dissolved oxygen, temperature and salinity on the dissolved oxygen consumption of the grass shrimp, Penaeus monodon. In: J.L. Maclean, L.B. Dizon and L.V. Hosillos (Editors), The First Asian Fisheries Forum. Asian Fisheries Society, Manila, Philippines, pp. 641-646. Mauro, N.A. and Mangum, C.P., 1982. The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. I. Interspecific responses to seasonal differences in temperature. J. Exp. Zool., 219: 179-188. Shigeno, K., 1979. Problems in Prawn Culture. Aquaculture Series 19. Balkema Press, Rotterdam, Netherlands, 103 pp. Smith, D.M. and Dall, W., 1985. Moult staging the tiger prawn Penaeus esculentus. In: P.C. Rothlisberg, B.J. Hill and D.J. Staples (Editors), Second Aust. Natl. Prawn Sem., 22-26 October 1984, NPS2, Cleveland, Australia, pp. 85-93. Taylor, E.W. and Whiteley, N.M., 1989. Oxygen transport and acid-base balance in the haemolymph of the lobster, Homarus gammarus, during aerial exposure and re-submersion. J. Exp. Biol., 144: 4 17-436. Truchot, J.P. and Jouve-Duhamel, A., 1983. Consommation d’oxygene de la crevette japonaise, Penaeusjaponicus, en fonction de l’oxygenation du milieu: effets de la temperature et de l’acclimatation a des conditions ambiantes hypoxiques. Bases biologiques de l’aquaculture. Montpellier, IFREMER Actes de Colloques, 1: 245-254. Van Donk, E. and De Wilde, P.A.W.J., 198 1. Oxygen consumption and motile activity of the brown shrimp Crangon crangun related to temperature and body size. Neth. J. Sea Res., 15: 54-64. Whiteley, N.M., Al-Wassia, A.H. and Taylor, E.W., 1990. The effect of temperature, aerial exposure and disturbance on oxygen consumption in the lobster, Homarus gammarus (L. ). Mar. Behav. Physiol., 17: 213-222. Winkler, P., 1987. Effects of handling on the in situ oxygen consumption of the American lobster (Homarus americanus). Comp. Biochem. Physiol., 87A: 69-7 1.