Skip to main content

Do parasites influence behavioural traits of wild and hatchery-reared Murray cod, Maccullochella peelii?

Parasitology Research volume 120, pages 515–523 (2021)Cite this article

Abstract

This study aimed to investigate the links between parasites and behavioural traits of juvenile Murray cod (Maccullochella peelii). The Murray cod is an endangered Australian freshwater fish for which restocking programs are in place and there is a growing human consumption market. However, little is known about the parasites of these fish and how these parasites influence their behaviour and survival. Fingerlings and yearling fish were sourced from a hatchery and the wild, and after acclimatisation in the laboratory, variation in behavioural traits was examined using emergence, exploration and predator inspection tests. The fish were then euthanised to determine their age and examined for infection with parasites. Wild fish had more camallanid nematodes and lernaeid copepods than hatchery fish. An information theoretic approach using Akaike’s Information Criterion (AIC) indicated that infection with protozoan cysts was an important factor for predicting the latency to emerge and explore a new environment, which was interpreted as reduced “boldness”. In contrast, the presence of lernaeid copepods was included in two of the four best models predicting predator inspection, indicating that infected fish were less likely to inspect a predator. Source of fish (wild or hatchery) was found to be a strong influence on behavioural responses in all our tests. All parasites found in the present study are known to result in clinical signs of diseases in their fish hosts, raising the possibility that responses in tests of behavioural traits reflect side effects of infection. Additionally, the effect of host adaptation to not show signs of parasite infection, or more simply that the effects on behaviour are subtle and difficult to reveal with small sample sizes, is discussed. Nonetheless, we propose that it is important that infection with parasites is considered in fish behavioural studies both to assess survival behaviour and to avoid misinterpretation of behavioural tests of animal personality.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Adams C, Huntingford F (2005) Behavioural syndromes in farmed fish: implications for production and welfare. Behaviour 142(9–10):1207–1221

    Article  Google Scholar 

  • Aghlmandi F, Habibi F, Afraii MA, Abdoli A, Shamsi S (2018) Infection with metacercaria of Clinostomum complanatum (Trematoda: Clinostomidae) in freshwater fishes from Southern Caspian Sea Basin. Revue de Médecine Vétérinaire 7:147–151

  • Allan BJM, Illing B, Fakan EP, Narvaez P, Grutter AS, Sikkel PC, McClure EC, Rummer JL, McCormick MI (2020) Parasite infection directly impacts escape response and stress levels in fish. J Exp Biol 223(16):jeb230904. https://doi.org/10.1242/jeb.230904

    Article  PubMed  Google Scholar 

  • Ashburner L (1978) Management and diseases of hatchery fishes. Post-Graduate Committee in Veterinary Science, University of Sydney

  • Ashburner L, Ehl A (1973) Chilodonella cyprini (Moroff), a parasite of freshwater fish and its treatment. Bull Aust Soc Limnol 5:3–4

    Google Scholar 

  • Barber I, Wright HA (2006) Effects of parasites on fish behaviour: interactions with host physiology. Fish Physiol 24:110–148

    Google Scholar 

  • Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10(2):131–165

    Article  Google Scholar 

  • Barber I, Walker P, Svensson PA (2004) Behavioural responses to simulated avian predation in female three spined sticklebacks: the effect of experimental Schistocephalus solidus infections. Behaviour 141:1425–1440. https://doi.org/10.1163/1568539042948231

    Article  Google Scholar 

  • Barber I, Mora A, Payne E, Weinersmith K, Sih A (2017) Parasitism, personality and cognition in fish. Behav Process 141:205–219

    CAS  Article  Google Scholar 

  • Behringer DC, Karvonen A, Bojko J (2018) Parasite avoidance behaviours in aquatic environments. Philos Trans R Soc Lond Ser B Biol Sci 373(1751):20170202. https://doi.org/10.1098/rstb.2017.0202

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretical approach, 2nd edn. Springer-Verlag, New York

    Google Scholar 

  • Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66(11):1543–1548. https://doi.org/10.1007/s00265-012-1416-2

    Article  Google Scholar 

  • Fernando CH, Furtado JI, Gussev AV, Hanek G, Kakonge SA (1972) Methods for the study of freshwater fish parasites, vol 12. University of Waterloo

  • Halliday RB, Collins RO (2002) Histiostoma papillata sp n. (Acari : Histiostomatidae), a mite attacking fish in Australia. Aust J Entomol 41:155–158. https://doi.org/10.1046/j.1440-6055.2002.00284.x

    Article  Google Scholar 

  • Hunt TL, Jones P (2018) Informing the great fish stocking debate: an Australian case study. Rev Fish Sci Aquacult 26(3):275–308

    Article  Google Scholar 

  • Huntingford FA (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. J Fish Biol 65:122–142. https://doi.org/10.1111/j.0022-1112.2004.00562.x

    Article  Google Scholar 

  • Hutchison M, Stewart D, Chilcott K, Butcher A, Henderson A, McLennan M, Smith P (2012) Strategies to improve post release survival of hatchery-reared threatened fish species. Murray–Darling Basin Authority Publ(135/11)

  • Ingram BA, Gavine FM, Lawson P (2005) Fish health management guidelines for farmed Murray cod. Department of Primary Industries

  • Jalali B, Shamsi S, Barzegar M (2005) Occurrence of Gyrodactylus spp (Monogenea: Gyrodactylidae) from Iranian freshwater fishes. Iranian Journal of Fisheries Sciences 4(2):19–30

  • Jones C (1986) Determining age of larval fish with the otolith increment technique. Fish Bull 84(1):91–104

    Google Scholar 

  • Karvonen A, Seppälä O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129(Pt 2):159–164. https://doi.org/10.1017/s0031182004005505

    CAS  Article  PubMed  Google Scholar 

  • Kekäläinen J, Lai Y-T, Vainikka A, Sirkka I, Kortet R (2014) Do brain parasites alter host personality? - Experimental study in minnows. Behav Ecol Sociobiol 68(2):197–204. https://doi.org/10.1007/s00265-013-1634-2

    Article  Google Scholar 

  • Kelley JL, Magurran AE, Macias-Garcia C (2005) The influence of rearing experience on the behaviour of an endangered Mexican fish, Skiffia multipunctata. Biol Conserv 122(2):223–230. https://doi.org/10.1016/j.biocon.2004.07.011

    Article  Google Scholar 

  • Kennedy C, Endler J, Poynton SL, McMinn H (1987) Parasite load predicts mate choice in guppies. Behav Ecol Sociobiol 21(5):291–295

    Article  Google Scholar 

  • Klemme I, Karvonen A (2016) Learned parasite avoidance is driven by host personality and resistance to infection in a fish–trematode interaction. Proc R Soc B Biol Sci 283(1838):20161148

    Article  Google Scholar 

  • Kuhn JA, Kristoffersen R, Knudsen R, Jakobsen J, Marcogliese DJ, Locke SA, Primicerio R, Amundsen P-A (2015) Parasite communities of two three-spined stickleback populations in subarctic Norway-effects of a small spatial-scale host introduction. Parasitol Res 114(4):1327–1339. https://doi.org/10.1007/s00436-015-4309-2

    Article  PubMed  Google Scholar 

  • Lafferty KD (2008) Ecosystem consequences of fish parasites. J Fish Biol 73(9):2083–2093

    Article  Google Scholar 

  • Landsberg J, Blakesley B, Reese R, McRae G, Forstchen P (1998) Parasites of fish as indicators of environmental stress. Environ Monit Assess 51(1–2):211–232

    Article  Google Scholar 

  • Larsson S, Linnansaari T, Vatanen S, Serrano I, Haikonen A (2011) Feeding of wild and hatchery reared Atlantic salmon (Salmo salar L.) smolts during downstream migration. Environ Biol Fish 92(3):361–369. https://doi.org/10.1007/s10641-011-9846-7

    Article  Google Scholar 

  • Lintermans M (2009) Fishes of the Murray-Darling Basin: an introductory guide. MDBC Publication No 10/07 © Murray-Darling Basin Authority 2009

  • Loot G, Lek S, Brown SP, Guegan JF (2001) Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda : Pseudophyllidea). J Parasitol 87(5):1002–1010

    CAS  Article  Google Scholar 

  • Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35(7):705–716. https://doi.org/10.1016/j.ijpara.2005.01.015

    Article  PubMed  Google Scholar 

  • McMinn H (2015) Effects of the nematode parasite Camallanus cotti on sexual and non-sexual behaviors in the guppy (Poecilia reticulata). Integr Comp Biol 30(2):245–249. https://doi.org/10.1093/icb/30.2.245

    Article  Google Scholar 

  • Mennerat A, Nilsen F, Ebert D, Skorping A (2010) Intensive farming: evolutionary implications for parasites and pathogens. Evol Biol 37(2):59–67. https://doi.org/10.1007/s11692-010-9089-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344(6264):330–333. https://doi.org/10.1038/344330a0

    Article  Google Scholar 

  • Mittelbach GG, Ballew NG, Kjelvik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71(6):927–944. https://doi.org/10.1139/cjfas-2013-0558

    Article  Google Scholar 

  • Molnár K, Rhode K (1988) New coccidians from fresh-water fishes of Australia. J Fish Dis 11(2):161–169. https://doi.org/10.1111/j.1365-2761.1988.tb00535.x

    Article  Google Scholar 

  • Molnár K, Székely C, Láng M (2019) Field guide to warmwater fish diseases in central and eastern Europe, the Caucasus and Central Asia. Food and Agriculture Organization of the United Nations

  • Palm HW, Ruckert S (2009) A new approach to visualize ecosystem health by using parasites. Parasitol Res 105(2):539–553. https://doi.org/10.1007/s00436-009-1423-z

    CAS  Article  PubMed  Google Scholar 

  • Peacock SJ, Krkosek M, Bateman AW, Lewis MA (2020) Estimation of spatiotemporal transmission dynamics and analysis of management scenarios for sea lice of farmed and wild salmon. Can J Fish Aquat Sci 77(1):55–68. https://doi.org/10.1139/cjfas-2019-0036

    Article  Google Scholar 

  • Philbey AW, Ingram BA (1991) Coccidiosis due to Goussia lomi (Protista, Apicomplexa) in aquarium-reared Murray cod, Maccullochella peeli (Mitchell), (Percichthyidae). J Fish Dis 14(2):237–242. https://doi.org/10.1111/j.1365-2761.1991.tb00593.x

    Article  Google Scholar 

  • Pittock J, Finlayson CM (2011) Australia’s Murray–Darling Basin: freshwater ecosystem conservation options in an era of climate change. Mar Freshw Res 62(3):232–243

    CAS  Article  Google Scholar 

  • Poulin R (1995) “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int J Parasitol 25(12):1371–1383. https://doi.org/10.1016/0020-7519(95)00100-x

    CAS  Article  PubMed  Google Scholar 

  • Poulin R (2011) Evolutionary ecology of parasites. Princeton university press

  • Poulin R (2013) Parasite manipulation of host personality and behavioural syndromes. J Exp Biol 216(1):18–26. https://doi.org/10.1242/jeb.073353

    Article  PubMed  Google Scholar 

  • Poulin R, Hammond-Tooke CA, Nakagawa S (2012) Parasitism and behavioural syndromes in the fish Gobiomorphus cotidianus. Behaviour 149(6):601–622

    Article  Google Scholar 

  • R Core Team, 2017, R: A language and environment for statistical com‐puting. Vienna, Austria: R Foundation for Statistical Computing

  • Rabe B, Gallego A, Wolf J, Murray ROH, Stuiver C, Price D, Johnson H (2020) Applied connectivity modelling at local to regional scale: the potential for sea lice transmission between Scottish finfish aquaculture management areas. Estuar Coast Shelf Sci 238. https://doi.org/10.1016/j.ecss.2020.106716

  • Railsback S, Harvey B (2011) Importance of fish behaviour in modelling conservation problems: food limitation as an example. J Fish Biol 79(6):1648–1662

    CAS  Article  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318

    Article  Google Scholar 

  • Reddacliff GL (1994) An update and overview on fish disease in Australia. Wildlife, The T G Hungerford Refresher Course for Veterinarians

  • Rowland SJ, Tully P (2004) Hatchery quality assurance program for Murray cod (Maccullochella peelii peelii), golden perch (Macquaria ambigua) and silver perch (Bidyanus bidyanus). NSW Department of Primary Industries

  • Rowland SJ, Ingram BA, Prokop FB (1991) Suspected cysts of the protozoan parasite Chilodonella hexasticha. Bull Eur Assoc Fish Pathol 11(4):159–161

    Google Scholar 

  • Sales E, Rogers L, Freire R, Kopf RK (2019) Links between behavioural traits, phenotype and life history in freshwater fish, Australian Freshwater Sciences Society Waurn Ponds, 1–4 December

  • Sarabian C, Curtis V, McMullan R (2018) Evolution of pathogen and parasite avoidance behaviours. The Royal Society

  • Shamsi S, Suthar J (2016) A revised method of examining fish for infection with zoonotic nematode larvae. Int J Food Microbiol 227:13–16. https://doi.org/10.1016/j.ijfoodmicro.2016.03.023

    Article  PubMed  Google Scholar 

  • Shamsi S, Zhu X, Barton DP, Dang M, Freire R, Nowak BF (2020) Dermocystidium sp. infection in farmed Murray cod, Maccullochella peelii. Aquaculture 528:735596. https://doi.org/10.1016/j.aquaculture.2020.735596

    CAS  Article  Google Scholar 

  • Shields RJ, Goode RP (1978) Host rejection of Lernaea cyprinacea L.(Copepoda). Crustaceana:301–307

  • Thiem JD, Wooden IJ, Baumgartner LJ, Butler GL, Forbes JP, Conallin J (2017) Recovery from a fish kill in a semi-arid Australian river: can stocking augment natural recruitment processes? Austral Ecol 42(2):218–226

    Article  Google Scholar 

  • Timi JT, Poulin R (2020) Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 50(10):755–761. https://doi.org/10.1016/j.ijpara.2020.04.007

    Article  PubMed  Google Scholar 

  • Toft C (1986) Communities of parasites with parasitic life-styles. Community Ecology (Diamond, JM and Case, TJ, eds):445-463, Harper & Row

  • Toms CN, Echevarria DJ, Jouandot DJ (2010) A methodological review of personality-related studies in fish: focus on the shy-bold axis of behavior. Int J Comp Psychol 23(1) Retrieved from https://escholarship.org/uc/item/949413qt

  • Vaughan GE, Coble DW (1975) Sublethal effects of three ectoparasites on fish. J Fish Biol 7(3):283–294

    Article  Google Scholar 

  • Ward AJW, Duff AJ, Krause J, Barber I (2005) Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala. Environ Biol Fish 72(2):155–160. https://doi.org/10.1007/s10641-004-9078-1

    Article  Google Scholar 

  • Whitaker JO Jr, Schlueter RA (1975) Occurence of the crustacean parasite, Lernaea cyprinacea, on fishes from the White River at Petersburg, Indiana. Am Midl Nat 93:446–450

    Article  Google Scholar 

  • Woo PTK (1995) Fish diseases and disorders. Volume 1: protozoan and metazoan infections fish diseases and disorders volume 1: protozoan and metazoan infections. CAB international, Wallingford. UK

  • Woo PTK, Shariff M (1990) Lernea cyprinacea L. (Copepoda: Caligidea) in Helostoma temmincki Cuvier & Valenciennes: the dynamics of resistance in recovered and naive fish. J Fish Dis 13(6):485–493. https://doi.org/10.1111/j.1365-2761.1990.tb00807.x

    Article  Google Scholar 

  • Zhu X, Barton DP, Wassens S, Shamsi S (2020) Morphological and genetic characterisation of the introduced copepod Lernaea cyprinacea, Linnaeaus (Cyclopoida: Lernaeidae) occurring in the Murrumbidgee catchment, Australia. Mar Freshw Res. https://doi.org/10.1071/MF20145

Download references

Acknowledgements

We are grateful to Dr. Di Barton from Charles Sturt University for her assistance in fish dissection, and Simon McDonald for statistical analysis.

Funding

This project was partially supported by Charles Sturt University (grant number A512-828-66770) and CSU Green.

Author information

Authors and Affiliations

  1. School of Animal and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW, 2650, Australia

    Shokoofeh Shamsi, Leia Rogers, Ellie Sales & Rafael Freire

  2. Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, NSW, 2650, Australia

    Shokoofeh Shamsi

  3. Institute for Land, Water and Society, Charles Sturt University, Albury, NSW, 2640, Australia

    Leia Rogers, R. Keller Kopf & Rafael Freire

Authors
  1. Shokoofeh Shamsi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leia Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ellie Sales
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Keller Kopf
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rafael Freire
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors have participated in (a) conception and design, or analysis and interpretation of the data; (b) drafting the article or revising it critically for important intellectual content; and (c) approval of the final version.

Corresponding author

Correspondence to Shokoofeh Shamsi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

This manuscript has not been submitted to, nor is under review at, another journal or other publishing venue.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Una Ryan

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shamsi, S., Rogers, L., Sales, E. et al. Do parasites influence behavioural traits of wild and hatchery-reared Murray cod, Maccullochella peelii?. Parasitol Res 120, 515–523 (2021). https://doi.org/10.1007/s00436-020-07021-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-07021-7

Keywords

  • Maccullochella peelii
  • Behaviour
  • Parasite
  • Personality