Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha)

Maule, A. G.; Tripp, R. A.; Kaattari, S. L.; Schreck, C. B.

doi:10.1677/joe.0.1200135

Cited by 330Aquaculture disease management and microbiotaStress Responses and CortisolReproductive biology and impacts on aquatic species

Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha)

Maule, A. G., Tripp, R. A., Kaattari, S. L., Schreck, C. B.·1989·Journal of Endocrinology

DOI 10.1677/joe.0.1200135

Open this paper in CoChat — free account

Abstract

We examined the effects of acute stress on the immune system and disease resistance of juvenile chinook salmon (Oncorhynchus tshawytscha) in laboratory and clinical trials. Immune function, as measured by the ability of lymphocytes from the anterior kidney to generate specific antibody-producing cells (APC) in vitro, was depressed 4 h after stress, when plasma cortisol levels were highest. At the same time, resistance to the fish pathogen, Vibrio anguillarum, was also depressed. Compared with controls, plasma cortisol and APC of stressed fish were unchanged after 24 h, and disease resistance was enhanced as evidenced by higher survival rate and longer mean time to death of mortalities. After 7 days, even though numbers of APC were depressed, plasma cortisol concentration and disease resistance did not differ from controls. This pattern was generally the same, independent of the type of stress applied: i.e. being held out of water in a dipnet for 30 s, manipulation during hatchery operations for 4 h, or transportation for 9 h. These and earlier findings suggest that similar endocrine-immune interactions operate in the mammalian and salmonid systems during acute stress. Journal of Endocrinology (1989) 120, 135–142

Integrity signals

Registry

Crossref · 10.1677/joe.0.1200135

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Allostatic overload can have a useful purpose for preservation of the species, such as in migrating salmon or the marsupial mouse, which die of excessive stress after mating.
“However, allostatic overload can also have a useful purpose for the preservation of the species, such as In migrating salmon or the marsupial mouse, which die of excessive stress after mating- the stress, and allostatic load, being caused for salmon, In part, by the migration up the rapidly flowing rivers, but also because of physiological changes that represent accelerated aging.12-14”
From Protective and damaging effects of stress mediators: central role of the brain (2006) · cites this paper as [13]

Sorted by citations

Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids
BARTON, B. A., & Iwama, G. K. (1991) · Annual Review of Fish Diseases · doi:10.1016/0959-8030(91)90019-g · Cited by 2,113 · see citing works
Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators
McEwen, B. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.071 · Cited by 1,864 · see citing works
“Yet, some types of allostatic overload can also have a useful purpose for the preservation of the species, such as in migrating salmon or the marsupial mouse, which die of excessive stress after mating — the stress, and allostatic load, being caused for salmon, in part, by the migration up the rapidly flowing rivers b…”
Background
Protective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/bmcewen · Cited by 1,220 · see citing works
Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes
HEMRE, G.-I., Mommsen, T. P., & Krogdahl, Å. (2002) · Aquaculture Nutrition · doi:10.1046/j.1365-2095.2002.00200.x · Cited by 895 · see citing works
Effects of stress on fish reproduction, gamete quality, and progeny
Schreck, C. B., Contreras‐Sánchez, W. M., & Fitzpatrick, M. S. (2001) · Aquaculture · doi:10.1016/s0044-8486(01)00580-4 · Cited by 637 · see citing works
Self-citation
Heat shock protein expression in fish
Iwama, G. K., Thomas, P. T., Forsyth, R., et al. (1998) · Reviews in Fish Biology and Fisheries · doi:10.1023/a:1008812500650 · Cited by 618 · see citing works
“The stress hormones activate a number of metabolic pathways that result in alterations in blood chemistry including plasma glucose concentration and haematology (Maule et al., 1989; Barton and Iwama, 1991; Randall and Perry, 1992; Vijayan et al., 1994, 1996, 1997b).”
Background
The Concept of Stress in Fish
Schreck, C. B., & Tort, L. (2016) · Fish physiology · doi:10.1016/b978-0-12-802728-8.00001-1 · Cited by 502 · see citing works
Self-citation
High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles
Montero, D., Izquierdo, M. S., Tort, L., et al. (1999) · Fish Physiology and Biochemistry · doi:10.1023/a:1007719928905 · Cited by 427 · see citing works
“High plasma cortisol levels produce an immunosuppresive effect in fish (Pickering and Pottinger 1985; Maule et al. 1989; Barton and Iwama 1991) reducing circulating lymphocytes (Pickering 1984; Ellsaesser and Clem 1987) and increasing the susceptibility of fish to disease (Pickering and Duston 1983; Houghton and Matth…”
BackgroundInfluential
The endocrine effects of mercury in humans and wildlife
Tan, S. W., Meiller, J., & Mahaffey, K. R. (2009) · Critical Reviews in Toxicology · doi:10.1080/10408440802233259 · Cited by 418 · see citing works
“These results suggest physiological endocrine dysfunction results from Hg exposure (Hontela et al., 1995), as cortisol has a regulatory role in reproduction, growth, osmoregulation, and the immune response in fish (Anderson et al., 1991; Donaldson, 1990; Maule et al., 1989).”
The efficacy of metomidate, clove oil, Aqui-S™ and Benzoak® as anaesthetics in Atlantic salmon (Salmo salar L.) smolts, and their potential stress-reducing capacity
Iversen, M. H., Finstad, B., McKinley, R. S., & Eliassen, R. A. (2003) · Aquaculture · doi:10.1016/s0044-8486(03)00111-x · Cited by 376 · see citing works
Behavioral and Neuroendocrine Correlates of Selection for Stress Responsiveness in Rainbow Trout--a Review
Øverli, Ø. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.3.463 · Cited by 348 · see citing works
“Fish under intensive culture conditions are exposed to a regime of acute and chronic stressors, which have adverse effects on growth, reproduction, immunocompetence, and flesh quality, among other things (Barton et al., 1987; Maule et al., 1989; Barton and Iwama, 1991; Lowe et al., 1993; Pickering, 1993; Balm, 1997; P…”
Background
Modulation of the fish immune system by hormones
Harris, J., & Bird, D. J. (2000) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(00)00235-x · Cited by 341 · see citing works
“In addition, cortisol decreases the activity of antibody producing cells and circulating titres of IgM (Maule et al., 1989; Nagae et al., 1994).”
BackgroundInfluential
Experimental control of stress hormone levels in fishes: techniques and applications
Gamperl, A. K., Vijayan, M. M., & Boutilier, R. G. (1994) · Reviews in Fish Biology and Fisheries · doi:10.1007/bf00044129 · Cited by 336 · see citing works
Stress in Fish
Iwama, G. K. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09005.x · Cited by 284 · see citing works
Whole-body cortisol response of zebrafish to acute net handling stress
Ramsay, J. M., Feist, G. W., Varga, Z. M., et al. (2009) · Aquaculture · doi:10.1016/j.aquaculture.2009.08.035 · Cited by 283 · see citing works
“Short-term increases in cortisol are believed to be adaptive, whereas repeated or chronic increases in cortisol are maladaptive resulting in decreased growth, impaired reproduction, and increased susceptibility to infectious diseases (Maule et al., 1989; Schreck et al., 2001; Saeij et al., 2003; Jentoft et al., 2005).”
BackgroundSelf-citation
Whole-body cortisol is an indicator of crowding stress in adult zebrafish, Danio rerio
Ramsay, J. M., Feist, G. W., Varga, Z. M., et al. (2006) · Aquaculture · doi:10.1016/j.aquaculture.2006.04.020 · Cited by 279 · see citing works
“The immediate response to stress is believed to be adaptive, allowing the organism to respond to the perceived threat, whereas chronic stress is considered to be maladaptive, with impacts on growth, reproduction and the immune response (Maule et al., 1989; Pickering, 1992; Schreck et al., 2001).”
BackgroundSelf-citation
Seasonal variations in the immune system of lower vertebrates
Zapata, A. G., Varas, A., & Torroba, M. (1992) · Immunology Today · doi:10.1016/0167-5699(92)90112-k · Cited by 273 · see citing works
Stress management in aquaculture: a review of dietary interventions
Ciji, A., & Akhtar, M. S. (2021) · Reviews in Aquaculture · doi:10.1111/raq.12565 · Cited by 268 · see citing works
Anesthetic efficacy of metomidate and comparison of plasma cortisol responses to tricaine methanesulfonate, quinaldine and clove oil anesthetized channel catfish Ictalurus punctatus
Small, B. C. (2003) · Aquaculture · doi:10.1016/s0044-8486(02)00302-2 · Cited by 233 · see citing works
“Severe or chronic stress is often associated with poor performance and has long been associated with immunosuppression in cultured fish (Pickering and Duston, 1983; Thomas and Lewis, 1987; Maule et al., 1989).”
Background
Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in juveniles
Kumar, S., Sahu, N. P., Pal, A. K., et al. (2005) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2005.03.001 · Cited by 232 · see citing works
Prevention of stress in rainbow trout (Oncorhynchus mykiss) fed diets containing different doses of glucan
Jeney, G., Galeotti, M., Volpatti, D., Jeney, Z., & Anderson, D. P. (1997) · Aquaculture · doi:10.1016/s0044-8486(97)00042-2 · Cited by 210 · see citing works
Recovery from loading and transport stress in Atlantic salmon (Salmo salar L.) smolts
Iversen, M. H., Finstad, B., & Nilssen, K. J. (1998) · Aquaculture · doi:10.1016/s0044-8486(98)00364-0 · Cited by 185 · see citing works
A Review of Stream Restoration Techniques and a Hierarchical Strategy for Prioritizing Restoration in Pacific Northwest Watersheds
Roni, P., Beechie, T. J., Bilby, R. E., Leonetti, F. E., Pollock, M. M., & Pess, G. R. (2002) · North American Journal of Fisheries Management · doi:10.1577/1548-8675(2002)022 · Cited by 623 · see citing works
The relationship between physiological stress and wildlife disease: consequences for health and conservation
Hing, S., Narayan, E. J., Thompson, R. C. A., & Godfrey, S. S. (2016) · Wildlife Research · doi:10.1071/wr15183 · Cited by 183 · see citing works
“Studies in laboratory animals (Dhabhar and McEwen 1997), livestock (Salak-Johnson and McGlone 2007), fish (Maule et al. 1989) and humans (Biondi and Zannino 1997) have indicated that stress can affect patterns of infectious disease (Sheridan et al.”
Background
Extracting fish size using dual underwater cameras
Costa, C., Loy, A., Cataudella, S., et al. (2006) · Aquacultural Engineering · doi:10.1016/j.aquaeng.2006.02.003 · Cited by 178 · see citing works
Plasma cortisol and glucose stress responses of red drum (Sciaenops ocellatus) to handling and shallow water stressors and anesthesia with MS-222, quinaldine sulfate and metomidate
Thomas, P., & Robertson, L. (1991) · Aquaculture · doi:10.1016/0044-8486(91)90140-3 · Cited by 172 · see citing works
Effect of vitamin E and C dietary supplementation on some immune parameters of gilthead seabream (Sparus aurata) juveniles subjected to crowding stress
Montero, D., Marrero, M. P., Izquierdo, M. S., et al. (1999) · Aquaculture · doi:10.1016/s0044-8486(98)00387-1 · Cited by 170 · see citing works
“Pickering and Pottinger, 1985; Maule et al., 1989 , resulting in an increase of Ž .susceptibility to diseases Barton and Iwama, 1991 .”
Background
Effects of Stress on the Reproductive Performance of Rainbow Trout (Oncorhynchus mykiss)1
Contreras‐Sánchez, W. M., Schreck, C. B., Fitzpatrick, M. S., & Pereira, C. B. (1998) · Biology of Reproduction · doi:10.1095/biolreprod58.2.439 · Cited by 166 · see citing works
“Several papers have demonstrated that when high levels of cortisol are present, the immune response of fish may be impaired [51-55].”
BackgroundSelf-citation
Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the ST. Lawrence river
Hontela, A., Dumont, P., Duclos, D., et al. (1995) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620140421 · Cited by 165 · see citing works
Protective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62128-7 · Cited by 158 · see citing works
Effects of chemical contaminants on blood chemistry of teleost fish: A bibliography and synopsis of selected effects
Folmar, L. C. (1993) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620120216 · Cited by 157 · see citing works
The effects of dietary organic or inorganic selenium in rainbow trout ( Oncorhynchus mykiss ) under crowding conditions
Küçükbay, F. Z., Yazlak, H., KARACA, I., et al. (2009) · Aquaculture Nutrition · doi:10.1111/j.1365-2095.2008.00624.x · Cited by 153 · see citing works
Depletion of serum alternative complement pathway activity in gilthead seabream caused by α-tocopherol and n-3 HUFA dietary deficiencies
Montero, D., Tort, L., Izquierdo, M. S., Robaina, L., & Vergara, J. M. (1998) · Fish Physiology and Biochemistry · doi:10.1023/a:1007734720630 · Cited by 148 · see citing works
“…hand, aquaculture conditions such as overcrowding or frequent handling has been reported to induce a stress response characterized by the release of the stress hormones (catecholamines and cortisol) with a subsequent depletion of the immune system (Pickering and Pottinger 1989; Maule et al. 1989).”
Background
Immunomodulation: Endogenous Factors
Schreck, C. B. (1996) · Fish physiology · doi:10.1016/s1546-5098(08)60278-2 · Cited by 148 · see citing works
Self-citation
Crowding stress induces changes in serum haemolytic and agglutinating activity in the gilthead sea bream Sparus aurata
Tort, L., Sunyer, J. O., Gómez, E., et al. (1996) · Veterinary Immunology and Immunopathology · doi:10.1016/0165-2427(95)05502-9 · Cited by 148 · see citing works
Stress responses in Atlantic salmon (Salmo salar L.) smolts during commercial well boat transports, and effects on survival after transfer to sea
Iversen, M. H., Finstad, B., McKinley, R. S., Eliassen, R. A., Carlsen, K. T., & Evjen, T. (2004) · Aquaculture · doi:10.1016/j.aquaculture.2004.10.019 · Cited by 146 · see citing works
Plasmatic levels of cortisol in the response to acute stress in Nile tilapia, Oreochromis niloticus (L.), previously exposed to chronic stress
Barcellos, L. J. G., Nicolaiewsky, S., de Souza, S. M. G., et al. (1999) · Aquaculture Research · doi:10.1046/j.1365-2109.1999.00348.x · Cited by 140 · see citing works
Multiple acute temperature stress affects leucocyte populations and antibody responses in common carp, Cyprinus carpio L.
Engelsma, M. Y. (2003) · Fish & Shellfish Immunology · doi:10.1016/s1050-4648(03)00006-8 · Cited by 140 · see citing works
The effect of dietary arachidonic acid on growth, survival, and cortisol levels in different-age gilthead seabream larvae (Sparus auratus) exposed to handling or daily salinity change
Koven, W., Anholt, R. D. V., Lutzky, S., Ben-Atia, I., Nixon, O., Ron, B., & Tandler, A. (2003) · Aquaculture · doi:10.1016/s0044-8486(03)00317-x · Cited by 137 · see citing works
The effect of stress on the immune response of Atlantic salmon (Salmo salar L.) fed diets containing different amounts of vitamin C
Thompson, I., White, A., Fletcher, T. C., et al. (1993) · Aquaculture · doi:10.1016/0044-8486(93)90246-u · Cited by 137 · see citing works
Stress and cortisol treatment changed affinity and number of glucocorticoid receptors in leukocytes and gill of coho salmon
Maule, A. G., & Schreck, C. B. (1991) · General and Comparative Endocrinology · doi:10.1016/0016-6480(91)90067-g · Cited by 136 · see citing works
Self-citation
Husbandry stress during early life stages affects the stress response and health status of juvenile sea bass, Dicentrarchus labrax
Varsamos, S., Flik, G., Pépin, J., Bonga, S. E. W., & Breuil, G. (2005) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2005.04.005 · Cited by 134 · see citing works
“stressor [ 45 ] and fish reared in high density, displayed higher mortality when”
Background
Time of day and water temperature modify the physiological stress response in green sturgeon, Acipenser medirostris
Lankford, S. E., Adams, T. E., & Cech, J. J. (2003) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(03)00075-8 · Cited by 132 · see citing works
Selection for high and low cortisol stress response in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss)
Fevolden, S. E., Refstie, T., & Røed, K. H. (1991) · Aquaculture · doi:10.1016/0044-8486(91)90072-f · Cited by 132 · see citing works
Biology of Bony Fish Macrophages
Hodgkinson, J. W., Grayfer, L., & Belosevic, M. (2015) · Biology · doi:10.3390/biology4040881 · Cited by 130 · see citing works
“Cortisol has been shown to immunosuppress fish and increase their susceptibility to diseases [192–194].”
Background
Serum haemolytic and agglutinating activity as indicators of fish immunocompetence: their suitability in stress and dietary studies
Tort, L., G�mez, E., Montero, D., et al. (1996) · Aquaculture International · doi:10.1007/bf00175219 · Cited by 125 · see citing works
“Thus, Ellsaesser and Clem (1986), Fries (1986), Maule et al. (1989) and Maule and Schreck (1990) showed reductions in several parameters such as circulating lymphocytes, mitogen activity and antibody production (plaque-forming cells, antibody-produci ng cells (APC) activity or rosette formation).”
Background
Effect of isoeugenol sedation on plasma cortisol, glucose, and lactate dynamics in channel catfish Ictalurus punctatus exposed to three stressors
Small, B. C. (2004) · Aquaculture · doi:10.1016/j.aquaculture.2004.05.021 · Cited by 125 · see citing works
“Stress induced elevations in plasma cortisol are known to suppress immunological capacity in salmonid fish (Maule et al., 1989; Pickering and Pottinger, 1989) and channel catfish (Davis et al., 2002, 2003), and increases in plasma glucose and lactate, indicative of glycogen mobilization and…”
Background
Effects of temperature change on the innate cellular and humoral immune responses of orange-spotted grouper Epinephelus coioides and its susceptibility to Vibrio alginolyticus
Cheng, A., Cheng, S.-A., Chen, Y.-Y., & Chen, J.-C. (2009) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2009.03.011 · Cited by 121 · see citing works
Effect of Dietary Supplementation with Vitamin E and Stocking Density on Macrophage Recruitment and Giant Cell Formation in the Teleost Fish, Piaractus mesopotamicus
Belo, M. A. D. A., Schalch, S. H. C., de Moraes, F. R., et al. (2005) · Journal of Comparative Pathology · doi:10.1016/j.jcpa.2005.04.004 · Cited by 121 · see citing works
Non-specific immune responses in the red porgy Pagrus pagrus after crowding stress
Rotllant, J., Pavlidis, M. A., Kentouri, M., et al. (1997) · Aquaculture · doi:10.1016/s0044-8486(97)00075-6 · Cited by 121 · see citing works
Anesthesia induces stress in Atlantic salmon (Salmo salar), Atlantic cod (Gadus morhua) and Atlantic halibut (Hippoglossus hippoglossus)
Zahl, I. H., Kiessling, A., Samuelsen, O. B., et al. (2009) · Fish Physiology and Biochemistry · doi:10.1007/s10695-009-9346-2 · Cited by 119 · see citing works
“These harmful effects from stress are related to elevated levels of corticosteroids, primarily cortisol (Barton and Iwama 1991; Maule et al. 1989; Mommsen et al. 1999; Pickering and Pottinger 1989).”
Background
Disease and Gill Lesions in Yellow Perch (Perca flavescens) Exposed to Oil Sands Mining-Associated Waters
van den Heuvel, M. R., Power, M., Richards, J. G., et al. (2000) · Ecotoxicology and Environmental Safety · doi:10.1006/eesa.1999.1912 · Cited by 119 · see citing works
Effects of dietary lipid level and vegetable oil on fatty acid metabolism in Atlantic salmon (Salmo salar L.) over the whole production cycle
Tocher, D. R., Bell, J. G., McGhee, F., et al. (2003) · Fish Physiology and Biochemistry · doi:10.1023/b:fish.0000045722.44186.ee · Cited by 119 · see citing works
“Other studies have shown changes in serum proteins, IgM levels and leucocyte populations, that may affect cellular and humoral immunity, take place around parr-smolt transformation in salmon (Maule et al. 1989; Melingen and Wergeland 2000; Melingen et al. 2002).”
Background
Utility of Splenic Macrophage Aggregates as an Indicator of Fish Exposure to Degraded Environments
Fournie, J. W., Summers, J. K., Courtney, L. A., Engle, V. D., & Blazer, V. S. (2001) · Journal of Aquatic Animal Health · doi:10.1577/1548-8667(2001)013 · Cited by 149 · see citing works
Physiological responses of hybrid striped bass under sedation by several anesthetics
Davis, K. B., & Griffin, B. R. (2003) · Aquaculture · doi:10.1016/j.aquaculture.2003.09.018 · Cited by 115 · see citing works
“Inhibition of the cortisol response consistently observed with metomidate is generally thought to prevent the immunosuppressive action of cortisol (Barton et al., 1987; Maule et al., 1989).”
BackgroundInfluential
The effects of stocking density and social interaction on acute stress response in Nile tilapia Oreochromis niloticus (L.) fingerlings
Barcellos, L. J. G., Nicolaiewsky, S., de Souza, S. M. G., & Lulhier, F. (1999) · Aquaculture Research · doi:10.1046/j.1365-2109.1999.00419.x · Cited by 113 · see citing works
Disease resistance in rainbow trout (Oncorhynchus mykiss) selected for stress response
Fevolden, S. E., Refstie, T., & Røed, K. H. (1992) · Aquaculture · doi:10.1016/0044-8486(92)90134-7 · Cited by 111 · see citing works
Nursery rearing of jundiá, Rhamdia quelen (Quoy & Gaimard) in cages: cage type, stocking density and stress response to confinement
Barcellos, L. J. G., Kreutz, L. C., Quevedo, R. M., et al. (2003) · Aquaculture · doi:10.1016/s0044-8486(03)00545-3 · Cited by 109 · see citing works
Dissolved Oxygen Level and Stocking Density Effects on Growth, Feed Utilization, Physiology, and Innate Immunity of Nile Tilapia, Oreochromis niloticus
Abdel‐Tawwab, M., Hagras, A. E., Elbaghdady, H. A. M., et al. (2014) · Journal of Applied Aquaculture · doi:10.1080/10454438.2014.959830 · Cited by 106 · see citing works
“High density causes changes in the immune system, and its impairment could lead to disease or death (Ellis et al. 2002; Maule et al. 1989; Mazur and Iwama 1993; Rotllant et al. 1997; Shreck 1990) Wise et al. (1993) found that confinement stress increased susceptibility of channel catfish to…”
Background
Pseudoloma neurophilia infections in zebrafish Danio rerio: effects of stress on survival, growth, and reproduction
Ramsay, J. M., Watral, V. G., Schreck, C., et al. (2009) · Diseases of Aquatic Organisms · doi:10.3354/dao02145 · Cited by 106 · see citing works
“Under conditions of chronic stress and elevation of cortisol, immune suppression is typical and often contributes to increased disease prevalence and morbidity in fish populations (Kent & Hedrick 1987, Maule et al. 1989, Saeij et al. 2003).”
Self-citation
Effects of sea lice (Lepeophtheirus salmonis Kröyer, 1837) infestation on macrophage functions in Atlantic salmon (Salmo salar L.)
Mustafa, A., MacWilliams, C., Fernandez, N. J., et al. (2000) · Fish & Shellfish Immunology · doi:10.1006/fsim.1999.0229 · Cited by 104 · see citing works
Artificial photoperiod influence on the immune system of juvenile rainbow trout (Oncorhynchus mykiss) in the Southern Hemisphere
Leonardi, M., & Klempau, A. E. (2003) · Aquaculture · doi:10.1016/s0044-8486(03)00032-2 · Cited by 104 · see citing works
The effect of various stresses, corticosteroids and adrenergic agents on phagocytosis in the rainbow trout Oncorhynchus mykiss
Narnaware, Y. K., Baker, B. I., & Tomlinson, M. G. (1994) · Fish Physiology and Biochemistry · doi:10.1007/bf00004117 · Cited by 104 · see citing works
“(Wedemeyer 1976; Barton et al. 1980; Walters and Plumb 1980; Weydemeyer and McLay 1981; Maule et al. 1989 ).”
Background
Management of Physiological Stress in Finfish Aquaculture
Davis, K. B. (2006) · North American Journal of Aquaculture · doi:10.1577/a05-007.1 · Cited by 103 · see citing works
“formation (Maule et al. 1989).”
Background
Temperature affects physiological stress responses to acute confinement in sunshine bass (Morone chrysops×Morone saxatilis)
Davis, K. B. (2004) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpb.2004.09.012 · Cited by 100 · see citing works
“Increased circulating cortisol has also been linked to immunosuppression (Maule et al., 1989).”
Background
The use of cleaner-fish to control sea lice on two Irish salmon (Salmo salar) farms with particular reference to wrasse behaviour in salmon cages
Deady, S., Varian, S. J. A., & Fives, J. M. (1995) · Aquaculture · doi:10.1016/0044-8486(94)00331-h · Cited by 100 · see citing works
Transport Stress Changes Blood Biochemistry, Antioxidant Defense System, and Hepatic HSPs mRNA Expressions of Channel Catfish Ictalurus punctatus
Refaey, M. M., & Li, D. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01628 · Cited by 102 · see citing works
“The stress resulted from transport often causes fish growth suppression, higher mortality (Akinrotimi, 2006), and the susceptibility to diseases (Maule et al., 1989), and the increment of rearing costs (Gomes et al., 2006).”
Background
Physiological response, blood chemistry profile and mucus secretion of red sea bream (Pagrus major) fed diets supplemented with Lactobacillus rhamnosus under low salinity stress
Dawood, M. A. O., Koshio, S., Ishikawa, M., et al. (2016) · Fish Physiology and Biochemistry · doi:10.1007/s10695-016-0277-4 · Cited by 97 · see citing works
Structural and functional impairment of the hypothalamo- pituitary-interrenal axis in fish exposed to bleached kraft mill effluent in the St Maurice River, Quebec
Hontela, A., Daniel, C., & Rasmussen, J. B. (1997) · Ecotoxicology · doi:10.1023/a:1018699405158 · Cited by 97 · see citing works
“Since cortisol has a role in regulation of metabolism, reproduction, growth and the immune function (Sheridan, 1986; Maule et al., 1989; Vijayan and Moon, 1992), disruption of normal cortisol secretion may have adverse secondary effects on fish health.”
The thymus in fish: Development and possible function in the immune response
Chilmonczyk, S. (1992) · Annual Review of Fish Diseases · doi:10.1016/0959-8030(92)90063-4 · Cited by 93 · see citing works
The Cost of Chronic Stress: Impacts of a Nonhabituating Stress Response on Metabolic Variables and Swimming Performance in Sturgeon
Lankford, S. E., Adams, T. E., Miller, R. A., & Cech, J. J. (2005) · Physiological and Biochemical Zoology · doi:10.1086/430687 · Cited by 90 · see citing works
Effect of handling stress on susceptibility of channel catfish Ictalurus punctatus to Ichthyophthirius multifiliis and channel catfish virus infection
Davis, K. B., Griffin, B. R., & Gray, W. L. (2002) · Aquaculture · doi:10.1016/s0044-8486(02)00362-9 · Cited by 89 · see citing works
“An increase in plasma cortisol is thought to be particularly important due to the immunosuppressive action of this hormone (Tripp et al., 1987; Maule et al., 1989).”
Background
Husbandry stress exacerbates mycobacterial infections in adult zebrafish, Danio rerio (Hamilton)
Ramsay, J. M., Watral, V. G., Schreck, C. B., & Kent, M. L. (2009) · Journal of Fish Diseases · doi:10.1111/j.1365-2761.2009.01074.x · Cited by 87 · see citing works
Self-citation
Glucocorticoid receptors in leukocytes and gill of juvenile coho salmon (Oncorhynchus kisutch)
Maule, A. G., & Schreck, C. B. (1990) · General and Comparative Endocrinology · doi:10.1016/0016-6480(90)90236-f · Cited by 87 · see citing works
Self-citation
Transportation stress affects performance of coho salmon, Oncorhynchus kisutch
Schreck, C. B., Solazzi, M. F., Johnson, S. L., et al. (1989) · Aquaculture · doi:10.1016/0044-8486(89)90391-8 · Cited by 84 · see citing works
Self-citation
Effects of fructooligosaccharide on immune response, antioxidant capability and HSP70 and HSP90 expressions of blunt snout bream (Megalobrama amblycephala) under high ammonia stress
Zhang, C., Li, X., Tian, H., et al. (2014) · Fish Physiology and Biochemistry · doi:10.1007/s10695-014-0017-6 · Cited by 82 · see citing works
Conditioning improves performance of juvenile chinook salmon, Oncorhynchus tshawytscha, to transportation stress
Schreck, C. B., Jónsson, L., Feist, G. W., et al. (1995) · Aquaculture · doi:10.1016/0044-8486(95)01018-1 · Cited by 82 · see citing works
Self-citation
Effect of handling and stocking density on hematocrit, plasma cortisol, and survival in wild and hatchery-reared chinook salmon (Oncorhynchus tshawytscha)
Mazur, C. F., & Iwama, G. K. (1993) · Aquaculture · doi:10.1016/0044-8486(93)90390-k · Cited by 82 · see citing works
Physiological responses and depression of humoral components of the immune system in gilthead sea bream (Sparus aurata) following daily acute stress
Sunyer, J. O., Gómez, E., Tort, L., et al. (1995) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f95-826 · Cited by 82 · see citing works
Mortality Estimates of Juvenile Spring–Summer Chinook Salmon in the Lower Columbia River and Estuary, 1992–1998: Evidence for Delayed Mortality?
Schreck, C. B., Stahl, T. P., Davis, L. E., Roby, D. D., & Clemens, B. J. (2006) · Transactions of the American Fisheries Society · doi:10.1577/t05-184.1 · Cited by 80 · see citing works
“Stress alters disease resistance in salmonids through effects on both immune system function and nonspecific resistance factors (Maule et al. 1989; Schreck et al. 1993; Schreck 1996).”
BackgroundInfluentialSelf-citation
Impaired cortisol secretion in yellow perch (Perca flavescens) from lakes contaminated by heavy metals: in vivo and in vitro assessment
Brodeur, J. C., Sherwood, G. D., Rasmussen, J. B., et al. (1997) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f97-200 · Cited by 81 · see citing works
“An impairment of cortisol secretion may also compromise the health of the fish because cortisol has a regulatory role in osmoregulation (Flick and Perry 1989; Madsen 1990), metabolism (Leach and Taylor 1982; Janssens and Waterman 1988), immune function (Pickering 1984; Maule et al. 1989), and reproduction (Wingfield a…”
Background
First-Year Cohort Dynamics and Overwinter Mortality of Juvenile Largemouth Bass
Jackson, J. R., & Noble, R. L. (2000) · Transactions of the American Fisheries Society · doi:10.1577/1548-8659(2000)129 · Cited by 14 · see citing works
Self-citation
Methodological Approaches and Opinions of Researchers Involved in the Surgical Implantation of Telemetry Transmitters in Fish
Wagner, G. N., & Cooke, S. J. (2005) · Journal of Aquatic Animal Health · doi:10.1577/h04-037.1 · Cited by 79 · see citing works
“This physiological disturbance can result in behavioral changes as well as an increased susceptibility to infection because of suppression of immune function (Pickering and Pottinger 1987; Maule et al. 1989; Mock and Peters 1990).”
Background
Effects of Early Rearing Environment on Stress Response, Immune Function, and Disease Resistance in Juvenile Coho (Oncorhynchus kisutch) and Chinook Salmon (O.tshawytscha)
Salonius, K., & Iwama, G. K. (1993) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f93-087 · Cited by 77 · see citing works
Automatic mass estimation of Jade perch Scortum barcoo by computer vision
Viazzi, S., Hoestenberghe, S. V., Goddeeris, B. M., et al. (2014) · Aquacultural Engineering · doi:10.1016/j.aquaeng.2014.11.003 · Cited by 76 · see citing works
Effects of high doses of cortisol on innate cellular immune response of seabream (Sparus aurata L.)
Esteban, M. Á., Rodriguez, A. C., Ayala, A. G., et al. (2004) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2004.02.006 · Cited by 75 · see citing works
Natural Changes in the Immune System of Fish
Tatner, M. F. (1996) · Fish physiology · doi:10.1016/s1546-5098(08)60276-9 · Cited by 75 · see citing works
Effects of thyroid hormone on the development of immune system in zebrafish
Lam, S. H., Lam, S. H., Sin, Y. M., et al. (2005) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2005.02.004 · Cited by 73 · see citing works
Effect of dietary vitamin E on growth, muscle composition, hematological and immunological parameters of sub-yearling beluga Huso huso L
Amlashi, A. S., Falahatkar, B., Sattari, M., & Gilani, M. H. T. (2011) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2011.01.002 · Cited by 73 · see citing works
Potential benefit of clove oil sedation on animal welfare during salmon smolt,Salmo salarL. transport and transfer to sea
Iversen, M. H., Eliassen, R. A., & Finstad, B. (2008) · Aquaculture Research · doi:10.1111/j.1365-2109.2008.02091.x · Cited by 69 · see citing works
Physiological responses of largemouth bass to acute temperature and oxygen stressors
VanLandeghem, M. M., Wahl, D. H., & Suski, C. D. (2010) · Fisheries Management and Ecology · doi:10.1111/j.1365-2400.2010.00740.x · Cited by 68 · see citing works
“Sublethal effects of elevated cortisol include suppression of immune function, which has been shown to increase the disease susceptibility of Chinook salmon, Oncorhynchus tshawytscha (Walbaum), during acute handling stressors (Maule et al. 1989).”
Background
Endocrine-induced pathology in stressed salmonid fish
Pickering, A. D. (1993) · Fisheries Research · doi:10.1016/0165-7836(93)90005-r · Cited by 68 · see citing works
Plasticity and constraint in response to early‐life stressors among late/final jomon period foragers from Japan: Evidence for life history trade‐offs from incremental microstructures of enamel
Temple, D. H. (2014) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22606 · Cited by 67 · see citing works
Effects of elevated temperature and nickel pollution on the immune status of Japanese medaka
Prophete, C., Carlson, E. A., Li, Y., et al. (2006) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2005.12.009 · Cited by 67 · see citing works
Disease resistance in Atlantic salmon (Salmo salar) selected for high or low responses to stress
Fevolden, S. E., Nordmo, R., Refstie, T., et al. (1993) · Aquaculture · doi:10.1016/0044-8486(93)90164-t · Cited by 67 · see citing works
In vitro effects of steroid hormones on IgM-secreting cells and IgM secretion in common carp (Cyprinus carpio)
SAHA, N., USAMI, T., & SUZUKI, Y. (2004) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2004.01.001 · Cited by 67 · see citing works
Suppression of immunological memory in juvenile chinook salmon (Oncorhynchus tshawytscha) from an urban estuary
Arkoosh, M. R., Casillas, E., Clemons, E., et al. (1991) · Fish & Shellfish Immunology · doi:10.1016/s1050-4648(05)80065-8 · Cited by 67 · see citing works
Effects of dietary carbohydrate sources on the growth performance and hepatic carbohydrate metabolic enzyme activities of juvenile cobia (Rachycentron canadum Linnaeus.)
Cui, X., Zhou, Q., Liang, H., et al. (2010) · Aquaculture Research · doi:10.1111/j.1365-2109.2010.02574.x · Cited by 66 · see citing works
Dietary nucleotide supplements influence the growth, haemato-immunological parameters and stress responses in endangered Caspian brown trout ( Salmo trutta caspius Kessler, 1877)
Kenari, A. A., Mahmoudi, N., Soltani, M., et al. (2012) · Aquaculture Nutrition · doi:10.1111/j.1365-2095.2012.00938.x · Cited by 65 · see citing works

A tool to identify pink salmon (Oncorhynchus gorbuscha)×Chinook salmon (O. tshawytscha) hybrids in the St. Marys River, Michigan–Ontario
Kennedy, A. J., Steinhart, G. B., & Greil, R. W. (2010) · Journal of Great Lakes Research · doi:10.1016/j.jglr.2010.04.007 · Cited by 2 · see citing works
Death Of A Salmon: An Investigation Of The Processes Affecting Survival And Migration Of Juvenile Yearling Chinook Salmon (Oncorhynchus Tshawytscha) In The Lower Columbia River And Ocean Plume
Brosnan, I. G. (2014) · eCommons (Cornell University) · Cited by 1 · see citing works
Establishment of Chinook salmon (Oncorhynchus tshawytscha) in Pacific basins of southern South America and its potential ecosystem implications
Soto, D., Arismendi, I., Prinzio, C. Y. D., et al. (2007) · Revista chilena de historia natural · doi:10.4067/s0716-078x2007000100007 · Cited by 110 · see citing works
Development of underwater recorders to quantify predation of juvenile Chinook salmon (Oncorhynchus tshawytscha) in a river environment
Demetras, N. J., Huff, D. D., Michel, C. J., et al. (2016) · Fishery Bulletin · doi:10.7755/fb.114.2.5 · Cited by 21 · see citing works
Genetic variation in chinook, Oncorhynchus tshawytscha , and coho, O. Kisutch
Reisenbichler, R. R., & Phelps, S. R. (1987) · Fishery Bulletin · Cited by 18 · see citing works

Authors: Maule, A. G., Tripp, R. A., Kaattari, S. L., & Schreck, C. B.
Affiliations: Oregon State University (US)
ORCID: Tripp, R. A.
Venue: Journal of Endocrinology
Publisher: Bioscientifica
Published: 1989-01-01
Volume: 120
Issue: 1
Pages: 135-142
ISSN: 0022-0795 (ISSN-L)
1479-6805
DOI: 10.1677/joe.0.1200135
OpenAlex: W2035540083
Cited by: 330
References: 0
Citations by year: 2026: 3 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 7 · 2018: 6 · 2017: 6 · 2016: 5 · 2015: 8 · 2014: 14 · 2013: 6 · 2012: 13
FWCI: 2.31
Type: journal article
Language: en
Open access: closed
Locations: Journal of Endocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords: acute stress, Oncorhynchus tshawytscha, immune function, disease resistance, cortisol, antibody-forming cells, Vibrio anguillarum, endocrine-immune interaction, fish handling stress, hatchery operations, transport stress
MeSH terms: Acute Disease, Animals, Antibody-Producing Cells, Cell Count, Hydrocortisone, Immunity, Innate, Salmon, Stress, Physiological, Time Factors, Vibrio Infections

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha)

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cited by

Related

Record

About these checks