The acute and chronic effect of low temperature on survival, heart rate and neural function in crayfish (Procambarus clarkii) and prawn (Macrobrachium rosenbergii) species

DOI: 10.4236/ojmip.2012.23011   PDF   HTML     4,884 Downloads   11,088 Views   Citations


The effect of acute and chronic cold exposure on heart rate (HR) and neuronal function in crayfish Procambarus clarkii and prawns Macrobrachium rosenbergii was addressed. This is particularly important since prawn farms of this species are used for aquaculture in varied climates world wide. The success of P. clarkii as an invasive species throughout the world may in part be due to their ability to acclimate to cold and warm habitats. A set of experiments was devised to address the physiological abilities of these species in managing rapid changes to cold environments as well as their ability to respond to sensory stimuli by using behavior and a bioindex of HR. Prawns died within 2 hrs when moved from 21℃ to 5℃. Crayfish reduced their HR but survived for at least a week with this rapid change. Changes in temperature of 5℃ each week resulted in death of the prawns when 10℃ was reached. Some died at 16℃ and some lasted at 10℃ for 1 day before dying. Crayfish remained responsive to sensory stimuli and survived with either rapid or slow changes in temperature from 21℃ to 5℃. Primary sensory neurons were rapidly inhibited in prawns with an acute change to 5℃, where as in crayfish the activity was reduced but not completely inhibited. An induced sensory-CNS-motor circuit elicited activity at neuromuscular junctions in prawns and crayfish at 21℃ but with acute changes to 5℃only in crayfish was the circuit functionally intact. The ability to survive rapid environmental temperature changes will impact survival and in time the distribution of a species. The significance of these findings is that they may account, in part, for the wide ecological distribution of P. clarkii as compared to M. rosenbergii. The invasiveness of organisms, as for P. clarkii, is likely linked to the physiological robustness to acute and chronic temperature changes of habitats.

Share and Cite:

Chung, Y. , Cooper, R. , Graff, J. and Cooper, R. (2012) The acute and chronic effect of low temperature on survival, heart rate and neural function in crayfish (Procambarus clarkii) and prawn (Macrobrachium rosenbergii) species. Open Journal of Molecular and Integrative Physiology, 2, 75-86. doi: 10.4236/ojmip.2012.23011.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Nystr?m, P. (1999) Ecological impact of introduced and native crayfish on freshwater communities: European perspectives. In: Gherardi, F. and Holdich, D.M., Eds., Crayfish in Europe as Alien Species—How to Make the Best of a Bad Situation? Balkema, Rotterdam, 63-85.
[2] Ackefors, H. (1999) The positive effects of established crayfish introductions in Europe. In: Gherardi, F. and Holdich, D.M., Eds., Crayfish in Europe as Alien Species —How to Make the Best of a Bad Situation? Balkema, Rotterdam, 49-61.
[3] García-Arberas, L., Rallo, A. and Antón, A. (2009) The future of the indigenous freshwater crayfish Austropotamobius italicus in Basque Country streams: Is it possible to survive being an inconvenient species? Knowledge and Management of Aquatic Ecosystems, 19, 394-395.
[4] Johnson, G.E. (1924) Giant nerve fibers in crustaceans with special reference to Cambarus and Palaemonetes. Journal of Comparative Neurology, 36, 323-373. doi:10.1002/cne.900360402
[5] Kennedy, D., Selverston, A.L. and Remler, M.P. (1969) Analysis of restricted neural networks. Science, 164, 14881496. doi:10.1126/science.164.3887.1488
[6] Krasne, F.B. and Winem J.J. (1975) Extrinsic modulation of crayfish escape behavior. Journal of Experimental Biology, 63, 433-450.
[7] Li, H., Listerman, L., Doshi, D. and Cooper, R.L. (2000) Use of heart rate to measure intrinsic state of blind cave crayfish during social interactions. Comparative Biochemistry and Physiology A, 127, 55-70. doi:10.1016/S1095-6433(00)00241-5
[8] Listerman, L., Deskins, J., Bradacs, H. and Cooper, R.L. (2000) Measures of heart rate during social interactions in crayfish and effects of 5-HT. Comparative Biochemistry and Physiology A, 125, 251-264. doi:10.1016/S1095-6433(99)00180-4
[9] Shuranova, Z.P., Burmistrov, Y.M., Strawn, J.R. and Cooper, R.L. (2006) Evidence for an autonomic nervous system in decapod crustaceans. International Journal of Zoological Research, 2, 242-283. doi:10.3923/ijzr.2006.242.283
[10] Hobbs, H.H. (1981) The crayfishes of Georgia. Smitsonian Contributions to Zoology, 318, 1-549. doi:10.5479/si.00810282.318
[11] Payette, A.L. and McGaw, I.J. (2003) Thermoregulatory behavior of the crayfish Procambarus clarki in a burrow environment. Comparative Biochemistry and Physiology A, 136, 539-556. doi:10.1016/S1095-6433(03)00203-4
[12] De Wachter, B.D. and McMahon, B.R. (1996) Temperature effects on heart performance and regional hemolymph flow in the crab Cancer magister. Comparative Biochemistry and Physiology A, 114, 27-33. doi:10.1016/0300-9629(95)02084-5
[13] Goudkamp, J.E., Seebacher, F., Ahern, M. and Franklin, C.E. (2004) Physiological thermoregulation in a crustacean? Heart rate hysteresis in the freshwater crayfish Cherax destructor. Comparative Biochemistry and Physiology A, 138, 399-403. doi:10.1016/j.cbpb.2004.06.002
[14] Jury, S.H., Watson, W.H. (2000) Thermosensitivity of the lobster, Homarus americanus, as determined by cardiac assay. Biological Bulletin, 199, 257-264. doi:10.2307/1543182
[15] Morris, S. and Taylor, A.C. (1984) Heart rate response of the intertidal prawn Palaemon elegans to simulated and in situ environmental changes. Marine Ecology Progress Series, 20, 127-136. doi:10.3354/meps020127
[16] Heitler, W.J. and Edwards, D.H. (1998) Effect of temperature on a voltage sensitive electrical synapse in crayfish. Journal of Experimental Biology, 201, 503-513.
[17] Nagayama, T. and Newland, P.L. (2011) Spontaneous motor nerve activity decreased with decreasing temperatures in crayfish. Temperature dependent plasticity of habituation in the crayfish. Journal of Comparative Physiology A, 197, 1073-1081. doi:10.1007/s00359-011-0668-z
[18] Cooper, R.M., Schapker-Finucane, H., Adami, H. and Cooper, R.L. (2011) Heart and ventilatory measures in crayfish during copulation. Open Journal of Molecular and Integrative Physiology, 1, 36-42. doi:10.4236/ojmip.2011.13006
[19] Somero, G.N., Dahloff, E. and Lin, J.J. (1996) Stenotherms and eurytherms: Mechanisms establishing thermal optima and tolerance ranges. In: Johnston, I. and Bennett, A., Eds., Animals and Temperature, Cambridge University Press, Cambridge, 53-77. doi:10.1017/CBO9780511721854.004
[20] Cooper, A.S. and Cooper, R.L. (2009) Historical view and physiological demonstration of synaptic transmission at the crayfish opener muscle. Journal of Visualized Experimentation, 33, e1959. doi:10.3791/1595
[21] McRae, T. (1999) Chemical removal of nitrite and chlorinating agents from municipal water supplies used for crayfish and aquarium finfish culture. In: Keller, M., Oidtmann, B., Hoffmann, R. and Vogt, G., Ed., Freshwater Crayfish 12, International Association of Astacology, Augsburg, 727-732.
[22] Bierbower, S.M. and Cooper, R.L. (2009) Measures of heart and ventilatory rates in freely moving crayfish. Journal of Visualized Experimentation, 32, e1594. doi:10.3791/1594
[23] Wilkens, J.L., Mercier, A.J. and Evans, J. (1985) Cardiac and ventilatory responses to stress and to neurohormonal modulators by the shore crab Carcinus maenas. Comparative Biochemistry and Physiology, 82, 337-343.
[24] Pagé, M.-P., Hailes, W. and Cooper, R.L. (2007) Modification of the tail flip escape response in crayfish by neuromodulation and behavioral state with and without descending CNS input. International Journal of Zoological Research, 3, 132-144.
[25] Cooper, R.L. and Ruffner, M.E. (1998) Depression of synaptic efficacy at intermolt in crayfish neuromuscular junctions by 20-Hydroxyecdysone, a molting hormone. Journal of Neurophysiology, 79, 1931-1941.
[26] Strawn, J.R., Neckameyer, W.S. and Cooper, R.L. (2000) The effects of 5-HT on sensory neurons, CNS command, and neuromuscular junctions of the crayfish abdominal superficial flexor. Comparative Biochemistry and Physiology B, 127, 533-550.
[27] Baierlein, B., Thurow, A.L., Atwood, H.L. and Cooper, R.L. (2011) Membrane potentials, synaptic responses, neuronal circuitry, neuromodulation and muscle histology using the crayfish: Student laboratory exercises. Journal of Visualized Experimentation, 47, e2325. doi:10.3791/2325
[28] Schapker, H., Breithaupt, T., Shuranova, Z., Burmistrov, Y. and Cooper, R.L. (2002) Heart rate and ventilatory correlative measures in crayfish during environmental disturbances & social interactions. Comparative Biochemistry and Physiology A, 131, 397-407.
[29] Shuranova, Z.P., Burmistrov, Y.M. and Cooper, R.L. (2003) Bioelectric field potentials of the ventilatory muscles in the crayfish. Comparative Biochemistry and Physiology A, 134, 461-469. doi:10.1016/S1095-6433(02)00322-7
[30] Frederich, M. and P?rtner, H.O. (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. American Journal of Physiology: Regulatory and Integrative Physiology, 279, R1531-R1538.
[31] Forward, R.B. (1990) Behavioural responses of crustacean larvae to rates of temperature change. Biological Bulletin, 178, 195-204. doi:10.2307/1541819
[32] Wine, J.J. and Krasne, F.B. (1982) The cellular organization of crayfish escape behavior. In: Sandeman, D.C. and Atwood, H.L., Eds., The Biology of Crustacea, Academic Press, New York, 241-292.
[33] Czajka, M.C. and Lee, R.E. (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. Journal of Experimental Biology, 148, 245-254.
[34] Graham, A.M., Merrill, J.D., McGaugh, S.E. and Noor, M.A. (2012) Geographic selection in the small heat shock gene complex differentiating populations of drosophila pseudoobscura. Journal of Heredity, 103, 400-407. doi:10.1093/jhered/esr150
[35] Vesala, L., Salminen, T.S., Laiho, A., Hoikkala, A. and Kankare, M. (2012) Cold tolerance and cold-induced modulation of gene expression in two Drosophila virilis group species with different distributions. Insect Molecular Biology, 21, 107-118. doi:10.1111/j.1365-2583.2011.01119.x
[36] Wheatly, M.G., Gao, Y., Stiner, I.M., Whalen, D.R., Nade, M., Vigo, F. and Golshani, A.E. (2007) Roles of NCX and PMCA in basolateral calcium export associated with mineralization cycles and cold acclimation in crayfish. Annals of the New York Academy of Sciences, 1099, 190-192. doi:10.1196/annals.1387.022
[37] White, A.J., Northcutt, M.J., Rohrback, S.E., Carpenter, R.O., Niehaus-Sauter, M.M., Gao, Y., Wheatly, M.G. and Gillen, C.M. (2011) Characterization of sarcoplasmic calcium binding protein (SCP) variants from freshwater crayfish Procambarus clarkii. Comparative Biochemistry and Physiology B, 160, 8-14. doi:10.1016/j.cbpb.2011.04.003
[38] Desai-Shah, M. and Cooper, R.L. (2009) Different mechanisms of Ca2+ regulation that influence synaptic transmission: Comparison between crayfish and Drosophila neuromuscular junctions. Synapse, 63, 1100-1121. doi:10.1002/syn.20695
[39] Desai-Shah, M. and Cooper, R.L. (2010) Actions of NCX, PMCA and SERCA on short-term facilitation and maintenance of transmission in nerve terminals. The Open Physiology Journal, 3, 37-50.
[40] Desai-Shah, M., Papoy, A.R., Ward, M. and Cooper, R.L. (2010) Roles of the SERCA, PMCA and NCX in calcium regulation in the Drosophila larval heart. The Open Physiology Journal, 3, 16-36. doi:10.2174/1874360901003010016
[41] Cossins, A.R. (1976) Changes in muscle lipid composition and resistance adaptation to temperature in the freshwater crayfish Austropotamobius pallipes. Lipids, 11, 307316. doi:10.1007/BF02544059
[42] Denlinger, D.L. and Lee, R.E. (1998) Physiology of cold sensitivity. In: Hallman, G.J. and Denlinger, D.L., Eds., Temperature Sensitivity in Insects and Application in Integrated Pest Management, Westview Press, Boulder, 5595.
[43] Nieminen, P., Paakkonen, T., Eeril?, H., Puukka, K., Riikonen, J., Lehto, V.P. and Mustonen, A.M. (2012) Freezing tolerance and low molecular weight cryoprotectants in an invasive parasitic fly, the deer ked (Lipoptena cervi). Journal of Experimental Zoology A: Ecological Genetic Physiology, 317, 1-8.
[44] Overgaard, J., S?rensen, J.G., Petersen, S.O., Loeschcke, V. and Holmstrup, M. (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology, 51, 1173-1182. doi:10.1016/j.jinsphys.2005.06.007
[45] Pruitt, N.L. (1998) Membrane lipid composition and overwintering strategy in thermally acclimated crayfish. American Journal of Physiology, 254, R870-R876.
[46] Guppy, M. and Withers, P. (1999) Metabolic depression in animals: Physiological perspectives and biochemical generalizations. Biology Review Cambridge Philosophical Society, 74, 1-40. doi:10.1017/S0006323198005258
[47] Wood, S.C. and Gonzales, R. (1996) Hypothermia in hypoxic animals: Mechanisms, mediators, and functional significance. Comparative Biochemistry and Physiology B, 113, 37-43. doi:10.1016/0305-0491(95)02045-4
[48] Field, L.H. and Larimer, J.L. (1975) The cardioregulatory system of crayfish: The role of circumoesophageal interneurones. Journal of Experimental Biology, 62, 531543.
[49] Field, L.H. and Larimer, J.L. (1975) The cardioregulatory system of crayfish: Neuroanatomy and physiology. Journal of Experimental Biology, 62, 519-530.
[50] Taylor, E.W. (1970) Spontaneous activity in the cardioaccelerator nerves of the crayfish, Astacus pallipes lereboullet. Comparative Biochemistry and Physiology, 33, 859-869. doi:10.1016/0010-406X(70)90034-4
[51] Wiersma, C.A.G. and Novitski, E. (1942) The mechanism of the nervous regulation of the crayfish heart. Journal of Experimental Biology, 19, 255-265.
[52] Van Harreveld, A. (1936) A physiological solution for freshwater crustaceans. Proceedings Society of Experimental Biology and Medicine, 34, 428-432.
[53] Cowan, D.F., Watson, W.H., Solow, A.R. and Mountcastle, A.M. (2007) Thermal histories of brooding lobsters, Homarus americanus, in the Gulf of Maine. Marine Biology, 150, 463-470. doi:10.1007/s00227-006-0358-5
[54] New, M.B., Valenti, W.C., Tidwell, J.H., D’Abramo, L.R. and Kutty, M.N. (2009) Freshwater prawns: Biology and farming. Wiley and Blackwell, Oxford, 1-560. doi:10.1002/9781444314649

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.