Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

The effect of parasitism by a blood-feeding isopod on the otolith chemistry of host fish

Elizabeth C. Heagney A D , Bronwyn M. Gillanders B and Iain M. Suthers C
+ Author Affiliations
- Author Affiliations

A School of Biological, Earth and Environmental Science, University of New South Wales, Sydney, NSW 2052, Australia.

B Southern Seas Ecology Laboratories, School of Earth & Environmental Sciences, University of Adelaide, Adelaide, SA 5005, Australia.

C Sydney Institute of Marine Science, 22 Chowder Bay Road, Mosman, NSW 2088, Australia.

D Corresponding author. Email: I.Suthers@unsw.edu.au

Marine and Freshwater Research 64(1) 10-19 https://doi.org/10.1071/MF12123
Submitted: 3 May 2012  Accepted: 18 September 2012   Published: 6 February 2013

Abstract

Otolith chemistry is widely used to discriminate fish stocks or populations, although many of the factors that determine trace-element concentrations within the otolith remain poorly understood. We investigated the effect of a blood-feeding isopod ectoparasite, Ceratothoa sp., on the otolith chemistry of yellowtail scad, Trachurus novaezelandiae. We sampled 65 fish from three subpopulations of T. novaezelandiae from Jervis Bay in south-eastern Australia, and used laser ablation (LA)–inductivelycoupled plasma mass spectrometry (ICPMS) to measure otolith lithium (Li) : calcium (Ca), magnesium (Mg) : Ca, strontium (Sr) : Ca and barium (Ba) : Ca from four consecutive summer and winter growth bands. Otoliths of parasitised fish were characterised by significantly lower Li : Ca and Mg : Ca, and higher Sr : Ca, than those of unparasitised individuals from the same subpopulation. The consistency of trends in otolith chemistry across ablation points and among subpopulations suggests that there is a consistent physiological mechanism through which Ceratothoa parasites affect the otolith chemistry of infected individuals. It is likely that a range of physical, metabolic, chemical and behavioural processes act in concert to influence the otolith chemistry of parasitised fish. Given the ubiquitous distribution of parasites in the marine environment, differential rates of parasitism among fish stocks, populations or migratory contingents may be an important but unappreciated factor driving stock- or population-based differences in otolith chemistry.

Additional keywords: Carangidae, Cymothoidae, ectoparasite, tongue biter.


References

Adlard, R. D., and Lester, R. J. G. (1995). The life cycle and biology of Anilocra pomacentri (Isopoda: Cymothoidae), an ectoparasitic isopod of the coral reef fish Chromis nitida (Perciformes: Pomacentridae). Australian Journal of Zoology 43, 271–281.
The life cycle and biology of Anilocra pomacentri (Isopoda: Cymothoidae), an ectoparasitic isopod of the coral reef fish Chromis nitida (Perciformes: Pomacentridae).Crossref | GoogleScholarGoogle Scholar |

Bath, G. E., Thorrold, S. R., Jones, C. M., Campana, S. E., McLaren, J. W., and Lam, J. W. H. (2000). Strontium and barium uptake in aragonitic otoliths of marine fish. Geochimica et Cosmochimica Acta 64, 1705–1714.
Strontium and barium uptake in aragonitic otoliths of marine fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjt1Sisrw%3D&md5=5d74ceb53157bf0d8c36d884b49d6087CAS |

Begg, G. A., and Waldman, J. R. (1999). An holistic approach to fish stock identification. Fisheries Research 43, 35–44.
An holistic approach to fish stock identification.Crossref | GoogleScholarGoogle Scholar |

Bergenius, M. A. J., Mapstone, B. D., Begg, G. A., and Murchie, C. D. (2005). The use of otolith chemistry to determine stock structure of three epinepheline serranid coral reef fishes on the Great Barrier Reef, Australia. Fisheries Research 72, 253–270.
The use of otolith chemistry to determine stock structure of three epinepheline serranid coral reef fishes on the Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar |

Bowman, T. E. (1960). Description and notes on the biology of Lironeca puhi, n.sp. (Isopoda: Cymothoidae), parasite of the Hawaiian moray eel, Gymnothorax eurostus (Abbott). Crustaceana 1, 84–91.
Description and notes on the biology of Lironeca puhi, n.sp. (Isopoda: Cymothoidae), parasite of the Hawaiian moray eel, Gymnothorax eurostus (Abbott).Crossref | GoogleScholarGoogle Scholar |

Bunkley-Williams, L., and Williams, E. H. (1998). Isopods associated with fishes: a synopsis and corrections. The Journal of Parasitology 84, 893–896.
Isopods associated with fishes: a synopsis and corrections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FgvVOmtQ%3D%3D&md5=58bbc7b59954516662e2bb0100357dccCAS |

Campana, S. E. (1999). Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series 188, 263–297.
Chemistry and composition of fish otoliths: pathways, mechanisms and applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtFKmtA%3D%3D&md5=962f7076537a4c0ef40321a452638d60CAS |

Campana, S. E., and Thorrold, S. R. (2001). Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Canadian Journal of Fisheries and Aquatic Sciences 58, 30–38.
Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations?Crossref | GoogleScholarGoogle Scholar |

Campana, S. E., Chouinard, G. A., Hanson, J. M., and Fréchet, A. (1999). Mixing and migration of overwintering Atlantic cod (Gadus morhua) stocks near the mouth of the Gulf of St Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 56, 1873–1881.

Campana, S. E., Chouinard, G. A., Hanson, J. M., Fréchet, A., and Brattey, J. (2000). Otolith elemental fingerprints as biological tracers of fish stocks. Fisheries Research 46, 343–357.
Otolith elemental fingerprints as biological tracers of fish stocks.Crossref | GoogleScholarGoogle Scholar |

Cuyás, C., Castro, J. J., Santana-Ortega, A. T., and Carbonell, E. (2004). Insular stock identification of Serranus atricauda (Pisces: Serranidae) through the presence of Ceratothoa steindachneri (Isopoda: Cymothoidae) and Pentacapsula cutanea (Myxozoa: Pentacapsulidae) in the Canary Islands. Scientia Marina 68, 159–163.

Elsdon, T. S., and Gillanders, B. M. (2004). Fish otolith chemistry influenced by exposure to multiple environmental variables. Journal of Experimental Marine Biology and Ecology 313, 269–284.
Fish otolith chemistry influenced by exposure to multiple environmental variables.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslGmur4%3D&md5=3121d2ebfa06b73f54979c44cea32dd8CAS |

Elsdon, T. S., and Gillanders, B. M. (2005). Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency. Canadian Journal of Fisheries and Aquatic Sciences 62, 1143–1152.
Alternative life-history patterns of estuarine fish: barium in otoliths elucidates freshwater residency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXoslGqs7o%3D&md5=b699f10e286b49615230439f570d343aCAS |

Elsdon, T. S., Wells, B. K., Campana, S. E., Gillanders, B. M., Jones, C. M., Limburg, K. E., Secor, D. H., Thorrold, S. R., and Walther, B. D. (2008). Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations, and inferences. Oceanography and Marine Biology: An Annual Review 46, 297–330.
Otolith chemistry to describe movements and life-history parameters of fishes: hypotheses, assumptions, limitations, and inferences.Crossref | GoogleScholarGoogle Scholar |

Ferrer-Castelló, E., Raga, J. A., and Aznar, F. J. (2007). Parasites as fish population tags and pseudoreplication problems: the case of striped red mullet Mullus surmuletus in the Spanish Mediterranean. Journal of Helminthology 81, 169–178.
Parasites as fish population tags and pseudoreplication problems: the case of striped red mullet Mullus surmuletus in the Spanish Mediterranean.Crossref | GoogleScholarGoogle Scholar |

Friedland, K. D., Reddin, D. G., Shimizu, N., Hass, R. E., and Youngson, A. F. (1998). Strontium: calcium ratios in Atlantic salmon (Salmo salar) otoliths and observations on growth and maturation. Canadian Journal of Fisheries and Aquatic Sciences 55, 1158–1168.
Strontium: calcium ratios in Atlantic salmon (Salmo salar) otoliths and observations on growth and maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtFOjsrs%3D&md5=107c409d049327b497aefbe977b3b2b3CAS |

Guthrie, J. F., and Kroger, R. L. (1974). Schooling habits of injured and parasitized menhaden. Ecology 55, 208–210.
Schooling habits of injured and parasitized menhaden.Crossref | GoogleScholarGoogle Scholar |

Hale, H. M. (1926). Review of Australian isopods of the cymothoid group. Part II. Transactions of the Royal Society of South Australia 50, 201–234.

Hayward, C. J., Perera, K. M. L., and Rohde, K. (1998). Assemblages of ectoparasites of a pelagic fish, slimy mackerel (Scomber australasicus), from south-eastern Australia. International Journal for Parasitology 28, 263–273.
Assemblages of ectoparasites of a pelagic fish, slimy mackerel (Scomber australasicus), from south-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7nsVWktg%3D%3D&md5=d3ba835697adc2bbad55229e190a920cCAS |

Horton, T., and Okamura, B. (2003). Post-haemorrhagic anaemia in sea bass, Dicentrarchus labrax (L.), caused by blood feeding of Ceratothoa oestroides (Isopoda: Cymothoidae). Journal of Fish Diseases 26, 401–406.
Post-haemorrhagic anaemia in sea bass, Dicentrarchus labrax (L.), caused by blood feeding of Ceratothoa oestroides (Isopoda: Cymothoidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svgs12ksQ%3D%3D&md5=1fdaa33ab16fdd299974a87c24bfad0cCAS |

Kalish, J. M. (1989). Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition. Journal of Experimental Marine Biology and Ecology 132, 151–178.
Otolith microchemistry: validation of the effects of physiology, age and environment on otolith composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpsFyktQ%3D%3D&md5=030a73ae6926aa41d72c8fe7904e7332CAS |

Kalish, J. M. (1991). Determinants of otolith chemistry: seasonal variation in the composition of blood plasma, endolymph and otoliths of bearded rock cod Pseudophycis barbatus. Marine Ecology Progress Series 74, 137–159.
Determinants of otolith chemistry: seasonal variation in the composition of blood plasma, endolymph and otoliths of bearded rock cod Pseudophycis barbatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslKhtrw%3D&md5=0deabcefe138a86b7be714ee5347483cCAS |

Kalish, J. M. (1992). Formation of a stress-induced chemical check in fish otoliths Journal of Experimental Marine Biology and Ecology 162, 265–277.
Formation of a stress-induced chemical check in fish otolithsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnslGitg%3D%3D&md5=d325d4e5fb98d614792712f50fac6673CAS |

Lanzing, W. J. R., and O’Connor, P. F. (1975). Infestation of Luderick (Girella tricuspidata) populations with parasitic isopods. Australian Journal of Marine and Freshwater Research 26, 355–361.
Infestation of Luderick (Girella tricuspidata) populations with parasitic isopods.Crossref | GoogleScholarGoogle Scholar |

Lester, R. J. G. (1990). Reappraisal of the use of parasites for fish stock identification. Australian Journal of Marine and Freshwater Research 41, 855–864.
Reappraisal of the use of parasites for fish stock identification.Crossref | GoogleScholarGoogle Scholar |

MacKenzie, K., and Abaunza, P. (1998). Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fisheries Research 38, 45–56.
Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods.Crossref | GoogleScholarGoogle Scholar |

Martin, G. B., and Thorrold, S. R. (2005). Temperature and salinity effects on magnesium, manganese, and barium incorporation in otoliths of larval and early juvenile spot Leiostomus xanthurus. Marine Ecology Progress Series 293, 223–232.
Temperature and salinity effects on magnesium, manganese, and barium incorporation in otoliths of larval and early juvenile spot Leiostomus xanthurus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps1CqtLw%3D&md5=72f2a283541c4a52c1823f2b4b027322CAS |

Martin, G. B., Thorrold, S. R., and Jones, C. M. (2004). Temperature and salinity effects on strontium incorporation in otoliths of larval spot (Leiostomus xanthurus). Canadian Journal of Fisheries and Aquatic Sciences 61, 34–42.
Temperature and salinity effects on strontium incorporation in otoliths of larval spot (Leiostomus xanthurus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjslylurw%3D&md5=8f9ab739460fce7bdf23b73b7416230fCAS |

Maxwell, J. G. H. (1982). Infestation of the jack mackerel, Trachurus declivis (Jenyns), with the cymothoid isopod, Ceratothoa imbricatus (Fabricus), in south eastern Australian waters. Journal of Fish Biology 20, 341–349.
Infestation of the jack mackerel, Trachurus declivis (Jenyns), with the cymothoid isopod, Ceratothoa imbricatus (Fabricus), in south eastern Australian waters.Crossref | GoogleScholarGoogle Scholar |

Otake, T., Ishii, T., Nakahara, M., and Nakamura, R. (1994). Drastic changes in otolith strontium/calcium ratios in leptocephali and glass eels of Japanese eel Anguilla japonica. Marine Ecology Progress Series 112, 189–193.
Drastic changes in otolith strontium/calcium ratios in leptocephali and glass eels of Japanese eel Anguilla japonica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitFSrtbw%3D&md5=35371433c5109a0f58a388ff862314f8CAS |

Payan, P., De Pontual, H., Edeyer, A., Borelli, G., Boeuf, G., and Mayer-Gostan, N. (2004). Effects of stress on plasma homeostasis, endolymph chemistry, and check formation during otolith growth in rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 61, 1247–1255.
Effects of stress on plasma homeostasis, endolymph chemistry, and check formation during otolith growth in rainbow trout (Oncorhynchus mykiss).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKnsbnP&md5=0ec8578ebc24ecb1f1c1bccb25e41d67CAS |

Perera, K. M. L. (1993). No evidence for seasonality in the ectoparasitic fauna of slimy mackerel, Scomber australasicus. Australian Journal of Marine and Freshwater Research 44, 709–719.
No evidence for seasonality in the ectoparasitic fauna of slimy mackerel, Scomber australasicus.Crossref | GoogleScholarGoogle Scholar |

Sadovy, Y., and Severin, K. P. (1994). Elemental patterns in red hind (Epinephelus guttatus) otoliths from Bermuda and Puerto Rico reflect growth rate, not temperature. Canadian Journal of Fisheries and Aquatic Sciences 51, 133–141.
Elemental patterns in red hind (Epinephelus guttatus) otoliths from Bermuda and Puerto Rico reflect growth rate, not temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXkslylu7s%3D&md5=0184891bf4b12bb32af9037d7dbe3597CAS |

Sievers, G., Lobos, C., Inostroza, R., and Ernst, S. (1996). The effect of the isopod parasite Ceratothoa gaudichaudii on the body weight of farmed Salmo salar in southern Chile. Aquaculture 143, 1–6.
The effect of the isopod parasite Ceratothoa gaudichaudii on the body weight of farmed Salmo salar in southern Chile.Crossref | GoogleScholarGoogle Scholar |

Stewart, J., and Ferrell, D. J. (2001). Age, growth and commercial landings of yellowtail scad (Trachurus novaezelandiae) and blue mackerel (Scomber australasicus) off the coast of New South Wales, Australia. New Zealand Journal of Marine and Freshwater Research 35, 541–551.
Age, growth and commercial landings of yellowtail scad (Trachurus novaezelandiae) and blue mackerel (Scomber australasicus) off the coast of New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Stewart, J., Ferrell, D. J., and Andrew, N. L. (1999). Validation of the formation and appearance of annual marks in the otoliths of yellowtail (Trachurus novaezelandiae) and blue mackerel (Scomber australasicus) in New South Wales. Marine and Freshwater Research 50, 389–395.
Validation of the formation and appearance of annual marks in the otoliths of yellowtail (Trachurus novaezelandiae) and blue mackerel (Scomber australasicus) in New South Wales.Crossref | GoogleScholarGoogle Scholar |

Suda, Y., Machii, T., and Orrego, H. (1995). Some fishery and biological aspects of jack mackerels, genus Trachurus (Carangidae). Scientia Marina 59, 571–580.

Tabachnick, B. G., and Fidell, L. S. (1983). ‘Using Multivariate Statistics.’ (Harper and Row: New York.)

Takagi, Y. (2002). Otolith formation and endolymph chemistry: a strong correlation between the aragonite saturation state and pH in the endolymph of the trout otolith organ. Marine Ecology Progress Series 231, 237–245.
Otolith formation and endolymph chemistry: a strong correlation between the aragonite saturation state and pH in the endolymph of the trout otolith organ.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeiurs%3D&md5=5228bd976c4b00940f8c2022ca5f4388CAS |

Thresher, R. E. (1999). Elemental composition of otoliths as a stock delineator in fishes. Fisheries Research 43, 165–204.
Elemental composition of otoliths as a stock delineator in fishes.Crossref | GoogleScholarGoogle Scholar |

Townsend, D. W., Radtke, R. L., Morrison, M. A., and Folsom, S. D. (1989). Recruitment implications of larval herring overwintering distributions in the Gulf of Maine, inferred using a new otolith technique. Marine Ecology Progress Series 55, 1–13.
Recruitment implications of larval herring overwintering distributions in the Gulf of Maine, inferred using a new otolith technique.Crossref | GoogleScholarGoogle Scholar |

Tzeng, W. N., Severin, K. P., and Wickström, H. (1997). Use of otolith chemistry to investigate the environmental history of European eel Anguilla anguilla. Marine Ecology Progress Series 149, 73–81.
Use of otolith chemistry to investigate the environmental history of European eel Anguilla anguilla.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjslWgu78%3D&md5=fd2d5419c06af839aa18b285687fe688CAS |