Abstract
Using a tame animal, the impact of otter (Lutra lutra) disturbance on over-wintering carp (Cyprinus carpio) was monitored in two experiments, 133 and 140 days, respectively, over two consecutive winters (November–April). The level of stress in over-wintering carp exposed to various intensities of disturbance by otters was quantified using biological indicators of stress (cortisol, cortisone, indices of nitrogen, carbohydrate, lipid and mineral metabolism and activity of basic blood plasma enzymes) taken from blood plasma of stocked carp at the end of the winter seasons (when the photoperiod was 12 light:12 dark, respectively, 13L:10D). Moreover, condition (Fulton’s coefficient of condition and fat content in muscles) and mortality rate of that carp were measured after over-wintering and also after the subsequent vegetation period. The analysis of blood and tissue samples of experimental fish showed changes in nitrogen, carbohydrate and mineral metabolism as well as levels of hormones and fat reserves. Higher response to stress in metabolism of carp with lower intensity of disturbance by otter suggests that high level of disturbance can lead to metabolic adaptation of carp to stress. The effect of stress on the mortality rate of carp during the over-wintering is not clear. Nevertheless, the negative effect of stress on survival, condition and growth rate of carp in the subsequent vegetation period was not observed.
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References
Adámek Z, Kortan D, Lepič P, Andreji J (2003) Impact of otter (Lutra lutra L.) predation on fishponds: a study of fish remains at ponds in the Czech Republic. Aqua Int 11:389–396
Balm PHM (1986) Osmoregulation in teleosts by cortisol and prolactin. Adaptation to low pH environments. Dissertation, University of Nijmegen, The Netherlands
Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the responses and effects of corticosteroids. Ann Rev Fish Dis 1:3–26
Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress in fish. In: Adams SM (ed) Biological indicators of aquatic ecosystem health. American Fisheries Society, Bethesda, pp 111–148
Bičíková M, Hampl R, Putz Z, Stárka L (1988) Comparison of isotope and nonisotope variants of direct cortisol immunoassay. In: Görög S (ed) Advances in steroid analysis. Akadémiai Kiadó, Budapest, pp 101–106
Bodner M (1998) Damage to stock in fish ponds as a result of otter (Lutra lutra L.) predation. BOKU-Reports on Wildlife Research & Game Management 14:106–117
Breves JP, Specker JL (2005) Cortisol stress response of juvenile winter flounder (Pseudopleuronectes americanus, Walbaum) to predators. J Exp Mar Biol Ecol 325:1–7
Cairns MA, Christian AR (1978) Effects of hemorrhagic stress on several blood parameters in adult rainbow trout, Salmo gairdneri. Trans Am Fish Soc 107:334–340
Campbell PM, Pottinger PT, Sumpter JP (1994) Preliminary evidence that chronic confinement stress reduces the quality of gametes produced by brown and rainbow trout. Aquaculture 120:151–169
Dabrowska H, Dabrowska K, Meyer-Burgdorff K, Hanke W, Gunthers KD (1991) The effect of large doses of vitamin C and magnesium on stress responses in common carp, Cyprinus carpio. Comp Biochem Physiol 99A:681–685
van Dijk PLM, van den Thillart GEEJM, Wendelaar Bonga SE (1993) Is there a synergistic effect between stead-state exercise and water acidification in carp? J Fish Biol 42:673–681
Engelsma MY, Hougee S, Nap D, Hofenk M, Rombout JHWM, van Muiswinkel WB, Verburg-van Kemenade LBM (2003) Multiple acute temperature stress affects leucocyte populations and antibody responses in common carp Cyprinus carpio L. Fish Shellfish Immunol 15:397–410
Farbridge KJ, Leatherland JF (1992) Plasma growth hormone levels in fed and fasted rainbow trout (Oncorhynchus mykiss) are decreased following handling stress. Fish Physiol Biochem 10:67–73
Gill TS, Pande J, Tewari H (1990) Sublethal effects of an organophosphorus insecticide on certain metabolite levels in a freshwater fish, Pontius conchonius Hamilton. Pest Biochem Physiol 36:290–299
Goos HJT, Consten D (2002) Stress adaptation, cortisol and pubertal development in the male common carp, Cyprinus carpio. Mol Cell Endocrinol 197:105–116
Järvi T (1990) Cumulative acute physiological stress in Atlantic salmon smolts: the effect of osmotic imbalance and the presence of predators. Aquaculture 89:337–350
Jørgensen EH, Vijayan MM, Aluru N, Maule AG (2002) Fasting modifies Aroclor 1254 impact on plasma cortisol, glucose and lactate responses to a handling disturbance in Arctic charr. Comp Biochem Physiol 132C:235–245
Kloskowski J (2005) Otter Lutra lutra damage at farmed fisheries in southeastern Poland. I. An interview survey. Wildlife Biol 11(3):201–206
Král J (1988) Studying the action of Menocain (Spofa), (3-aminobenzoic acid ethylester sodium hydrogen sulphate), a new anaesthetic for fish. Biol Chem Factors Anim Prod Vet 24:101–109
Kranz A (1995) On the ecology of otters in Central Europe. Dissertation, Institute of Wildlife Biology and Game Management, BOKU Vienna, Austria
Kranz A (2000) Otters (Lutra lutra) increasing in Central Europe: from the threat of extinction to locally perceived overpopulation? Mammalia 64:357–368
Lusková V, Svoboda M, Kolářová J (2002) The effect of diazinon on blood plasma biochemistry profile in common carp (Cyprinus carpio L.). Acta Vet Brno 71:117–123
Mazeaud MM, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with a general review. Trans Am Fish Soc 106:201–212
Moberg GP (2000) Physiological response to stress: implications for animal welfare. In: Moberg GP, Mench JA (eds) The biology of animal stress. CABI Publishing, New York, pp 1–21
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action and metabolic regulation. Rev Fish Biol Fish 9:211–268
Myšiak J, Schwerdtner K, Ring I (2004) Comparative analysis of the conflicts between carp pond farming and the protection of otters (Lutra lutra) in Upper Lusatia and South Bohemia. UFZ series: Discussion paper, Leipzig. http://www.ufz.de/data/ufz-disk8-20041829.pdf
Natarajan GM (1989) Changes in the carbohydrate metabolites during acute and chronic exposure of air-breathing fish Channa striatus to oxydemeton methyl (metasystox). Comp Physiol Ecol 14:181–184
Navrátil S, Páliková M, Vajcová V (1998) The effect of pure microcystin LR and biomas of blue-green algae on blood indices of carp (Cyprinus carpio L.). Acta Vet Brno 67:273–279
Patino R, Schreck CB, Redding JM (1985) Clearance of plasma corticosteroids during smoltification of coho salmon, Oncorhynchus kisutch. Comp Biochem Physiol 82A:531–535
Patino R, Redding JM, Schreck CB (1987) Interrenal secretion of corticosteroids and plasma cortisol and cortisone concentrations after acute stress and during seawater acclimation in juvenile coho salmo (Oncorhynchus kisutchi). Gen Comp Endocrinol 68:431–439
Pickering AD (ed) (1981) Stress and fish. Academic Press, New York
Pickering AD (1990) Stress and the suppression of somatic growth in teleost fish. In: Epple A, Scanes CG, Stetson MH (eds) Progress in comparative endocrinology. Wiley-Liss, New York, pp 473–479
Pickering AD, Pottinger TG (1995) Biochemical effects of stress. In: Hochachka PW, Mommsen TP (eds) Environmental and ecological biochemistry. Elsevier, Amsterdam, pp 349–379
Poledník L (2005) Otters and fishponds in the Czech Republic: interactions and consequences. Dissertation, Palacky University, Olomouc, Czech Republic
Pottinger TG (1998) Changes in blood cortisol, glucose and lactate in carp retained in anglers’ keepnets. J Fish Biol 53:728–742. DOI 10.1111/j.1095-8649.1998.tb01828.x
Pottinger TG, Moran TA (1993) Differences in plasma cortisol and cortisone dynamics during stress in two strains of rainbow trout (Oncorhynchus mykiss). J Fish Biol 43:121–130
Pottinger TG, Yeomans WE, Carrick TR (1999) Plasma cortisol and 17β-oestradiol levels in roach exposed to acute and chronic stress. J Fish Biol 54:525–532. DOI 10.1111/j.1095-8649.1999.tb00633.x
Pottinger TG, Rand-Weaver M, Sumpter JP (2003) Overwintering fasting and re-feeding in rainbow trout: plasma growth hormone and cortisol levels in relation to energy mobilisation. Comp Biochem Physiol 136B:403–417
Rehnberg BG, Schreck CB (1987) Chemosensory detection of predators by coho salmon (Oncorhynchus kisutch): behavioral reaction and the physiological stress response. Can J Zool 65:481–485
Roelants I, Epler P, Mikolajczyk T, Sokolowska-Mikolajczyk M, Breton B, Ollevier F (1993) The effect of handling stress on the circadian release pattern of cortisol and gonadotropin (GTH2) in female carp (Cyprinus carpio L.). Pol Arch Hydrobiol 40:347–353
Ruane NM (2002) Stress and stress disorders in a teleost fish, the common carp Cyprinus carpio L. Dissertation, Wageningen University, The Netherlands
Ruane NM, Huisman EA, Komen J (2001) Plasma cortisol and metabolite level profiles in two isogenic strains of common carp during confinement. J Fish Biol 59:1–12. DOI 10.1111/j.1095-8649.2001.tb02334.x
Ruane NM, Huisman EA, Komen J (2002) The influence of feeding history on the acute stress response of common carp Cyprinus carpio L. Aquaculture 210:245–257
Sancho E, Ferrando MD, Andrev E (1997) Sublethal effects of an organophosphate insecticide on the European eel, Anguilla anguilla. Ecotoxicol Environ Safety 36:57–65
Schreck CB (1981) Stress and compensation in teleostean fishes: response to social and physical factors. In: Pickering AD (ed) Stress and fish. Academic Press, New York, pp 295–321
Singh HH, Srivastava AK (1982) Effect of formothion on carbohydrate metabolism in Indian catfish (Heteropneustes fossilis). Environ Res 28:335–339
Smart GR (1981) Aspect of water quality producing stress in intensive fish culture. In: Pickering AD (ed) Stress and fish. Academic Press, New York, pp 277–293
Srivastava AK (1981) Effects of acute exposure of methyl parathion on carbohydrate metabolism of Indian catfish (Heteropneustes fossilis). Acta Pharmacol Toxicol 48:26–34
StatSoft, Inc. (1999) STATISTICA for Windows [Computer program manual] Tulsa, USA
Svobodová Z, Kaláb L, Dušek B, Vykusová B, Kolářová J, Janoušková D (1999) The effect of handling and transport on the concentration of glucose and cortisol in blood plasma of common carp. Acta Vet Brno 68:265–274
Vierhapper H, Derfler K, Nowotny P, Hollenstein U, Waldhausl W (1991) Impaired conversion of cortisol to cortisone in chronic renal insufficiency – a cause of hypertension or an epiphenomenon? Acta Endocrinol 125:160–164
Vijayan MM, Mommsen TP, Glémet HC, Moon TW (1996) Metabolic effects of cortisol treatment in a marine teleost, the sea raven. J Exp Biol 199:1509–1514
Waring CP, Stagg RM, Poxton MG (1996) Physiological responses to handling in the turbot. J Fish Biol 48:161–173
Wedemeyer GA (1983) Physiological effects of handling and hauling stress on smallmouth bass, Micropterus dolomieui. Prog Fish-Culturist 45:110–112
Wedemeyer GA (1997) Effects of rearing conditions on the health and physiological quality of fish in intensive culture. In: Iwama GK, Pickering AD, Sumpter JP, Shreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 35–71
Wedemeyer GA, Barton BA, McLeay DJ (1990) Stress and acclimation. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 451–489
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625
Woodley CM, Peterson MS (2003) Measuring responses to simulated predation threat using behavioral and physiological metrics: the role of aquatic vegetation. Behav Ecol 136:155–160
Wysocki LE, Dittami JP, Ladich F (2006) Ship noise and cortisol secretion in European freshwater fishes. Biol Conserv 128:501–508
Yin Z, Lam TJ, Sin YM (1995) The effects of crowding stress on the non-specific immune response in fancy carp (Cyprinus carpio L.). Fish Shellfish Immunol 5:519–529
Zar JH (1999) Biostatistical analysis. Prentice Hall, New Jersey
Acknowledgements
We would like to thank everyone from the Otter Station in Pavlov and Petra Hlaváčová, who helped with experiments and who took care of the tame otters. We also thank Klaus Hackländer, Jim Conroy and Richard Hampl for valuable comments on an draft of the manuscript. Finally, we are grateful to Hartmut Gossow. The project was financed by the European Commission (project no. EVK2-CT-2002-00142).
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Poledník, L., Řehulka, J., Kranz, A. et al. Physiological responses of over-wintering common carp (Cyprinus carpio) to disturbance by Eurasian otter (Lutra lutra). Fish Physiol Biochem 34, 223–234 (2008). https://doi.org/10.1007/s10695-007-9180-3
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DOI: https://doi.org/10.1007/s10695-007-9180-3
Keywords
- Cortisol
- Cortisone
- Predator–prey interaction
- Stress