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Stress response of Salmo salar (Linnaeus 1758) when heavily infested by Caligus rogercresseyi (Boxshall & Bravo 2000) copepodids

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Abstract

The year-round presence of ovigerous females of the parasite Caligus rogercresseyi in the fish farms of southern Chile results in a continuous source of the copepodid (infestive) stage of this louse. The short generation time in spring–summer could lead to high abundances of this copepodid, potentially leading to high infestation levels for fish. Knowing how heavy lice infestations affect Salmo salar can help determine how to time antiparasitic treatments so as to both minimize the treatment impact and reduce lice infestation levels for fish. This study aimed to describe the effects of high infestations of the copepodid stage of C. rogercresseyi on the physiology of S. salar. Two groups of S. salar were used: an infested group (75 copepodids per fish) and a control group (not infested). Sixty-five days after the first infestation, the infested fish group was re-infested at an infestation pressure of 200 copepodids per fish. Sampling was done prior to and following the second infestation, at 56 and 67 days (the latter 2 days following the second infestation). Several physiological variables were measured: cortisol (primary stress response) and glucose, proteins, amino acids, triglycerides, lactate, osmolality levels, and number and diameter of skin mucous cells (secondary stress responses). The plasma cortisol, glucose, and triglyceride levels were altered in the heavily infested fish, as was the diameter of skin mucous cells. These results suggest that heavy infestations of C. rogercresseyi lead to an acute stress response, metabolic reorganization, and increased mucus production in S. salar under heavy infestation conditions.

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Abbreviations

Dpfi:

Days post first infestation

Dpsi:

Days post second infestation

IP:

Infestation pressure

References

  • Ansari RA, Rahman S, Kaur M, Anjum S, Raisuddin S (2011) In vivo cytogenetic and oxidative stress-inducing effects of cypermethrin in freshwater fish, Channa punctata Bloch. Ecotoxicol Environ Saf 74:150–156. doi:10.1016/j.ecoenv.2010.08.036

    Article  CAS  PubMed  Google Scholar 

  • Barton B (2000) Salmonid fishes differ in their cortisol and glucose responses to handling and transport stress. N Am J Aquac. doi:10.1577/1548-8454(2000)062<0012:SFDITC>2.0.CO;2

    Google Scholar 

  • Bowers JM, Mustafa A, Speare DJ, Conboy GA, Brimacombe M, Sims DE, Burka JF (2000) The physiological response of Atlantic salmon, Salmo salar L., to a single experimental challenge with sea lice, Lepeophtheirus salmonis. J Fish Dis 23:165–172. doi:10.1046/j.1365-2761.2000.00225.x

    Article  Google Scholar 

  • Bowers JM, Speare DJ, Burka JF (2002) The effects of hydrogen peroxide on the stress response of Atlantic Salmon (Salmo salar). J Vet Pharmacol Ther 25:311–313. doi:10.1046/j.1365-2885.2002.00413.x

    Article  CAS  PubMed  Google Scholar 

  • Boxshall GA, Bravo S (2000) On the identity of the common Caligus (Copepoda: Siphonostomatoida: Caligidae) from salmonid netpen systems in southern Chile. Contrib Zool 69:137–146

    Google Scholar 

  • Buchmann K, Bresciani J (1998) Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitol Res 84:17–24. doi:10.1007/s004360050350

    Article  CAS  PubMed  Google Scholar 

  • Buchmann K, Bresciani J, Jappe C (2004) Effects of formalin treatment on epithelial structure and mucous cell densities in rainbow trout, Oncorhynchus mykiss (Walbaum), skin. J Fish Dis 27:99–104. doi:10.1111/j.1365-2761.2003.00519.x

    Article  CAS  PubMed  Google Scholar 

  • Carvajal J, González L, George-Nascimento M (1998) Native sea lice (Copepoda: Caligidae) infestation of salmonids reared in netpen systems in southern Chile. Aquaculture 166:241–246. doi:10.1016/S0044-8486(98)00301-9

    Article  Google Scholar 

  • Costello MJ (2006) Ecology of sea lice parasitic on farmed and wild fish. Trends Parasitol 22:475–483. doi:10.1016/j.pt.2006.08.006

    Article  PubMed  Google Scholar 

  • Costello MJ (2009) The global economic cost of sea lice to the salmonid farming industry. J Fish Dis 32:115–118. doi:10.1111/j.1365-2761.2008.01011.x

    Article  PubMed  Google Scholar 

  • Ellis T, Yildiz HY, Lopez-Olmeda J, Spedicato MT, Tort L, Overli O, Martins CI (2012) Cortisol and finfish welfare. Fish Physiol Biochem 38:163–188. doi:10.1007/s10695-011-9568-y

    Article  CAS  PubMed  Google Scholar 

  • Fast MD et al (2002) Susceptibility of rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis. Dis Aquat Org 52:57–68. doi:10.3354/dao052057

    Article  PubMed  Google Scholar 

  • Fast MD, Muise DM, Easy RE, Ross NW, Johnson SC (2006) The effects of Lepeophtheirus salmonis infections on the stress response and immunological status of Atlantic salmon (Salmo salar). Fish Shellfish Immunol 21:228–241. doi:10.1016/j.fsi.2005.11.010

    Article  CAS  PubMed  Google Scholar 

  • Fast MD, Hosoya S, Johnson SC, Afonso LOB (2008) Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immunol 24:194–204. doi:10.1016/j.fsi.2007.10.009

    Article  CAS  PubMed  Google Scholar 

  • Foss A, Grimsbø E, Vikingstad E, Nortvedt R, Slinde E, Roth B (2012) Live chilling of Atlantic salmon: physiological response to handling and temperature decrease on welfare. Fish Physiol Biochem 38:565–571. doi:10.1007/s10695-011-9536-6

    Article  CAS  PubMed  Google Scholar 

  • González L, Carvajal J (2003) Life cycle of Caligus rogercresseyi, (Copepoda: Caligidae) parasite of Chilean reared salmonids. Aquaculture 220:101–117. doi:10.1016/s0044-8486(02)00512-4

    Article  Google Scholar 

  • González MP, Marín SL, Vargas-Chacoff L (2015) Effects of Caligus rogercresseyi (Boxshall and Bravo, 2000) infestation on physiological response of host Salmo salar (Linnaeus 1758): establishing physiological thresholds. Aquaculture 438:47–54. doi:10.1016/j.aquaculture.2014.12.039

    Article  Google Scholar 

  • Heath AG (1995) Water pollution and fish physiology. CRC Press, Florida

    Google Scholar 

  • Helgesen K, Bravo S, Sevatdal S, Mendoza J, Horsberg T (2014) Deltamethrin resistance in the sea louse Caligus rogercresseyi (Boxhall and Bravo) in Chile: bioassay results and usage data for antiparasitic agents with references to Norwegian conditions. J Fish Dis 37:877–890. doi:10.1111/jfd.12223

    Article  CAS  PubMed  Google Scholar 

  • Hemre GI, Mommsen TP, Krogdahl Å (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194. doi:10.1046/j.1365-2095.2002.00200.x

    Article  CAS  Google Scholar 

  • Heuch P, Nordhagen J, Schram T (2000) Egg production in the salmon louse (Lepeophtheirus salmonis (Krøyer)) in relation to origin and water temperature. Aquac Res 31:805–814. doi:10.1046/j.1365-2109.2000.00512.x

    Article  Google Scholar 

  • Holm H, Santi N, Kjøglum S, Perisic N, Skugor S, Evensen Ø (2015) Difference in skin immune responses to infection with salmon louse (Lepeophtheirus salmonis) in Atlantic salmon (Salmo salar L.) of families selected for resistance and susceptibility. Fish Shellfish Immunol 42:384–394. doi:10.1016/j.fsi.2014.10.038

    Article  CAS  PubMed  Google Scholar 

  • Jung-Hoon J, Masroor F, Ju-Chan K (2005) Responses of cypermethrin-induced stress in haematological parameters of Korean rockfish, Sebastes schlegeli (Hilgendorf). Aquac Res 36:898–905. doi:10.1111/j.1365-2109.2005.01299.x

    Article  Google Scholar 

  • Krasnov A, Skugor S, Todorcevic M, Glover KA, Nilsen F (2012) Gene expression in Atlantic salmon skin in response to infection with the parasitic copepod Lepeophtheirus salmonis, cortisol implant, and their combination. BMC Genom 13:130. doi:10.1186/1471-2164-13-130

    Article  CAS  Google Scholar 

  • Krkošek M, Bateman A, Proboszcz S, Orr C (2010) Dynamics of outbreak and control of salmon lice on two salmon farms in the Broughton Archipelago, British Columbia. Aquac Environ Interact 1:137–146. doi:10.3354/aei00014

    Article  Google Scholar 

  • Lower N, Moore A (2003) Exposure to insecticides inhibits embryo development and emergence in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 28:431–432. doi:10.1023/B:FISH.0000030617.74673.92

    Article  CAS  Google Scholar 

  • Marín SL, Martin R, Lewis R (2015) Effects of Caligus rogercresseyi (Boxshall & Bravo 2000) chalimus stage condition (dead, moribund, live) on the estimates of Cypermethrin BETAMAX® efficacy. Aquac Res 46:30–36. doi:10.1111/are.12460

    Article  Google Scholar 

  • Meyer C, Ganter M, Korting W, Steinhagen D (2002) Effects of a parasite-induced nephritis on osmoregulation in the common carp Cyprinus carpio. Dis Aquat Org 50:127–135

    Article  PubMed  Google Scholar 

  • Moberg GP, Mench JA (2000) The biology of animal stress: basic principles and implications for animal welfare. CABI Publishing, New York

    Book  Google Scholar 

  • Molinari N, Daurés JP, Durand JF (2001) Regression splines for threshold selection in survival data analysis. Stat Med 20:237–247. doi:10.1002/1097-0258(20010130)20:2<237:AID-SIM654>3.0.CO;2-I

    Article  CAS  PubMed  Google Scholar 

  • Molinet C et al (2011) Population dynamic of early stages of Caligus rogercresseyi in an embayment used for intensive salmon farms in Chilean inland seas. Aquaculture 312:62–71. doi:10.1016/j.aquaculture.2010.12.010

    Article  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. doi:10.1023/A:1008924418720

    Article  Google Scholar 

  • Nolan DT, Reilly P, Wendelaar Bonga SE (1999) Infection with low numbers of the sea louse Lepeophtheirus salmonis induces stress-related effects in postsmolt Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 56:947–959. doi:10.1139/f99-021

    Article  Google Scholar 

  • Olafsdottir SH, Buchmann K (2004) Dexamethasone treatment affects skin mucous cell density in Gyrodactylus derjavini infected Salmo salar. J Helminthol 78:87–90. doi:10.1079/JOH2003206

    Article  CAS  PubMed  Google Scholar 

  • Olsvik PA, Ørnsrud R, Lunestad BT, Steine N, Fredriksen BN (2014) Transcriptional responses in Atlantic salmon (Salmo salar) exposed to deltamethrin, alone or in combination with azamethiphos. Comp Biochem Phys C 162:23–33. doi:10.1016/j.cbpc.2014.03.005

    CAS  Google Scholar 

  • Pankhurst N, Ludke S, King H, Peter R (2008) The relationship between acute stress, food intake, endocrine status and life history stage in juvenile farmed Atlantic salmon, Salmo salar. Aquaculture 275:311–318. doi:10.1016/j.aquaculture.2008.01.001

    Article  CAS  Google Scholar 

  • Pittman K et al (2013) Body site matters: an evaluation and application of a novel histological methodology on the quantification of mucous cells in the skin of Atlantic salmon, Salmo salar L. J Fish Dis 36:115–127. doi:10.1111/jfd.12002

    Article  CAS  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Redding JM, Patiño R, Schreck CB (1984) Clearance of corticosteroids in yearling coho salmon, Oncorhynchus kisutch, in fresh water and seawater and after stress. Gen Comp Endocrinol 54:433–443. doi:10.1016/0016-6480(84)90159-X

    Article  CAS  PubMed  Google Scholar 

  • Russ JC, DeHoff RT (2000) Practical stereology, vol 1. Kluwer Academic/Plenum, New York

    Book  Google Scholar 

  • Sandodden R, Finstad B, Iversen M (2001) Transport stress in Atlantic salmon (Salmo salar L.): anaesthesia and recovery. Aquac Res 32:87–90. doi:10.1046/j.1365-2109.2001.00533.x

    Article  CAS  Google Scholar 

  • SERNAPESCA (2014) Aprueba Tratamiento coordinado de invierno contra Caligidosis. Ministerio de Economía Fomento y Turismo, Valparaíso

    Google Scholar 

  • Shea E, Vecchione M (2002) Quantification of ontogenetic discontinuities in three species of oegopsid squids using model II piecewise linear regression. Mar Biol 140:971–979. doi:10.1007/s00227-001-0772-7

    Article  Google Scholar 

  • Skjervold PO, Fjæra SO, Østby PB, Einen O (2001) Live-chilling and crowding stress before slaughter of Atlantic salmon (Salmo salar). Aquaculture 192:265–280. doi:10.1016/S0044-8486(00)00447-6

    Article  Google Scholar 

  • Sutherland B, Koczka K, Yasuike M, Jantzen S, Yazawa R, Koop B, Jones S (2014) Comparative transcriptomics of Atlantic Salmo salar, chum Oncorhynchus keta and pink salmon O. gorbuscha during infections with salmon lice Lepeophtheirus salmonis. BMC Genom 15(1):200. doi:10.1186/1471-2164-15-200

    Article  Google Scholar 

  • Treasurer JW, Bravo S (2011) The spatial distribution patterns of Caligus rogercresseyi and C. elongatus on Atlantic salmon hosts (Salmo salar). Aquaculture 320:154–158. doi:10.1016/j.aquaculture.2011.03.032

    Article  Google Scholar 

  • Tseng Y-C, Hwang P-P (2008) Some insights into energy metabolism for osmoregulation in fish. Comp Biochem Phys C 148:419–429. doi:10.1016/j.cbpc.2008.04.009

    Google Scholar 

  • Tucker CS, Sommerville C, Wootten R (2000) The effect of temperature and salinity on the settlement and survival of copepodids of Lepeophtheirus salmonis (Krøyer, 1837) on Atlantic salmon, Salmo salar L. J Fish Dis 23:309–320. doi:10.1046/j.1365-2761.2000.00219.x

    Article  Google Scholar 

  • Ucán-Marín F, Ernst W, O’Dor RK, Sherry J (2012) Effects of food borne ivermectin on juvenile Atlantic salmon (Salmo salar L.): Survival, growth, behavior, and physiology. Aquaculture 334–337:169–175. doi:10.1016/j.aquaculture.2011.12.036

    Article  Google Scholar 

  • Vargas-Chacoff L, Arjona FJ, Polakof S, del Rio MP, Soengas JL, Mancera JM (2009) Interactive effects of environmental salinity and temperature on metabolic responses of gilthead sea bream Sparus aurata. Comp Biochem Physiol Part A Mol Integr Physiol 154:417–424. doi:10.1016/j.cbpa.2009.07.015

    Article  Google Scholar 

  • Vargas-Chacoff L et al (2011) Growth performance, osmoregulatory and metabolic modifications in red porgy fry, Pagrus pagrus, under different environmental salinities and stocking densities. Aquac Res 42:1269–1278. doi:10.1111/j.1365-2109.2010.02715.x

    Article  CAS  Google Scholar 

  • Vargas-Chacoff L et al (2014a) Combined effects of high stocking density and Piscirickettsia salmonis treatment on the immune system, metabolism and osmoregulatory responses of the sub-Antarctic Notothenioid fish Eleginops maclovinus. Fish Shellfish Immunol 40:424–434. doi:10.1016/j.fsi.2014.07.024

    Article  CAS  PubMed  Google Scholar 

  • Vargas-Chacoff L, Moneva F, Oyarzún R, Martínez D, Muñoz JLP, Bertrán C, Mancera JM (2014b) Environmental salinity-modified osmoregulatory response in the sub-Antarctic notothenioid fish Eleginops maclovinus. Polar Biol 37:1235–1245. doi:10.1007/s00300-014-1515-9

    Article  Google Scholar 

  • Vargas-Chacoff L et al (2014c) Stocking density and Piscirickettsia salmonis infection effect on Patagonian blennie (Eleginops maclovinus, Cuvier 1830) skeletal muscle intermediate metabolism. Fish Physiol Biochem 40:1683–1691. doi:10.1007/s10695-014-9959-y

    Article  CAS  PubMed  Google Scholar 

  • Vargas-Chacoff L, Ruiz-Jarabo I, Páscoa I, Gonçalves O, Mancera JM (2014d) Yearly growth and metabolic changes in earthen pond-cultured meagre. Sci Mar 78:193–202. doi:10.3989/scimar.03965.06B

    Article  Google Scholar 

  • Vatsos I, Kotzamanis Y, Henry M, Angelidis P, Alexis M (2010) Monitoring stress in fish by applying image analysis to their skin mucous cells. Eur J Histochem EJH 54:107–111. doi:10.4081/ejh.2010.e22

    Google Scholar 

  • Vijayan MM, Ballantyne JS, Leatherland JF (1990) High stocking density alters the energy metabolism of brook charr, Salvelinus fontinalis. Aquaculture 88:371–381. doi:10.1016/0044-8486(90)90162-G

    Article  Google Scholar 

  • Wedemeyer G (1996) Physiology of fish in intensive culture systems, 1st edn. Springer, Dordrecht

    Book  Google Scholar 

  • Wells A et al (2006) Physiological effects of simultaneous, abrupt seawater entry and sea lice (Lepeophtheirus salmonis) infestation of wild, sea-run brown trout (Salmo trutta) smolts. Can J Fish Aquat Sci 63:2809–2821. doi:10.1139/f06-160

    Article  CAS  Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  • Wood CM (1991) Acid–base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J Exp Biol 160:285–308

    CAS  Google Scholar 

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Acknowledgments

The authors want to thank the Instituto de Fomento Pesquero for supporting this study, Marine Harvest Chile for providing experimental fish, and FONDECYT 1110235. M.P. González is funded by Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) with a National Doctoral Scholarship and wants to thank the Fish Physiology Laboratory and LINTEC Laboratory of Universidad Austral de Chile.

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Authors and Affiliations

  1. Programa de Doctorado en Ciencias de la Acuicultura, Universidad Austral de Chile, Los Pinos s/n, Balneario Pelluco, Puerto Montt, Chile

    Margarita P. González

  2. Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Independencia 641, Valdivia, Chile

    Luis Vargas-Chacoff

  3. Instituto de Acuicultura, Universidad Austral de Chile, Los Pinos s/n, Balneario Pelluco, Puerto Montt, Chile

    Margarita P. González & Sandra L. Marín

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  1. Margarita P. González
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  2. Luis Vargas-Chacoff
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Correspondence to Margarita P. González.

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González, M.P., Vargas-Chacoff, L. & Marín, S.L. Stress response of Salmo salar (Linnaeus 1758) when heavily infested by Caligus rogercresseyi (Boxshall & Bravo 2000) copepodids. Fish Physiol Biochem 42, 263–274 (2016). https://doi.org/10.1007/s10695-015-0134-x

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