Skip to main content
SpringerLink
Log in

Ectoparasite infestation and host–parasite trophic relationship for Champsocephalus gunnari (Lonnberg, 1905) at South Orkney Islands, Antarctica

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

An analysis of ectoparasite infestations in Champsocephalus gunnari at South Orkney Islands, Antarctica, was performed, which revealed the prevalence, mean abundance, and mean intensity of the two species of parasites collected. The parasites’ preference for parts of the infested host fish was also investigated. The host–parasite trophic relationship was further examined using stable carbon and nitrogen isotopic analysis. The results showed that Eubrachiella antarctica was more inclined to parasitize the fins of C. gunnari. The carbon isotope ratio (δ13C) of the host was negatively correlated with the values for carbon isotopic discrimination (Δδ13C) between host and E. antarctica. The relationship between E. antarctica and C. gunnar is considered “parasitic” because E. antarctica has a higher trophic level than that of host C. gunnari, while Trulliobdella capitis may be a carrier parasite of C. gunnari or show a “symbiotic” relationship with it. The ecological niche spaces of the three species do not overlap, indicating the existence of specific trophic niches in the marine food web.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets created during and/or analyzed during the current study are available in the supplementary materials and other data can be required from the corresponding author upon reasonable request.

References

  • Behrmann-Godel J, Yohannes E (2015) Multiple isotope analyses of the pike tapeworm Triaenophorus nodulosus reveal peculiarities in consumer-diet discrimination patterns. J Helminthol 89:238–243

    Article  CAS  PubMed  Google Scholar 

  • Bielecki A, Rokicka M, Ropelewska E, Dziekonska-Rynko J (2008) Leeches [Hirudinida: Piscicolidae]-parasites of Antarctic fish from Channichthyidae family. Wiad Parazytol 54:345–348

    PubMed  Google Scholar 

  • Brinkmann A (1948) Some new and remarkable leeches from the Antarctic seas. Sci Results Norw Antarctic Exped 1927-1928, I Kommisjon Hos Jacob Kybwad Oslo 29:1-20

  • Campbell LM, Hecky RE, Wandera SB (2003) Stable isotope analyses of food web structure and fish diet in Napoleon and Winam Gulfs, Lake Victoria. East Africa J Great Lakes Res 29:243–257

    Article  CAS  Google Scholar 

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453

    Article  CAS  Google Scholar 

  • Deudero S, Pinnegar JK, Polunin NV (2002) Insights into fish host-parasite trophic relationships revealed by stable isotope analysis. Dis Aquat Organ 52:77–86

    Article  PubMed  Google Scholar 

  • Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? P Natl Acad Sci USA 105:11482–11489

    Article  CAS  Google Scholar 

  • Doucett RR, Giberson DJ, Power G (1999) Parasitic association of Nanocladius (Diptera: Chironomidae) and Pteronarcys biloba (Plecoptera: Pteronarcyidae): insights from stable-isotope analysis. J N Am Benthol Soc 18:514–523

    Article  Google Scholar 

  • Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris AM, Martinez ND, McLaughlin JP, Mouritsen KN, Poulin R, Reise K (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLOS Biol 11:e1001579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hebert CE, Shutt JL, Hobson KA, Weseloh DC (1999) Spatial and temporal differences in the diet of Great Lakes herring gulls (Larus argentatus): evidence from stable isotope analysis. Can J Fish Aquat Sci 56:323–338

    Article  Google Scholar 

  • Hecky R, Hesslein R (1995) Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. J N Am Benthol Soc 14:631–653

    Article  Google Scholar 

  • Huxham M, Raffaelli D, Pike A (1995) Parasites and food web patterns. J Anim Ecol 168–176

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER-stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602

    Article  PubMed  Google Scholar 

  • Jakubowski M (1971) Bia3okrwisto æ i inne osobliwo ci ichtiofauny Antarktyki [White-blooded-ness and other peculiarities of the Antarctic ichthyofauna]. Przegl Zool 15:262–272

    Google Scholar 

  • Janusz J, Sosinski J (1999) Eubrachiella antractica [Quidor, 1906] [Copepoda]-levels of infection in selected fish species of the family Nototheniidae. Acta Ichthyol Piscat 29:43–52

    Article  Google Scholar 

  • Johnson PT, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371

    Article  PubMed  Google Scholar 

  • Jones C, Damerau M, Deitrich K, Driscoll R, Kock K-H, Kuhn K, Moore J, Morgan T, Near T, Pennington J (2009) Demersal finfish survey of the South Orkney Islands. NOAA Tech Memo NMFS SWFSC 445:49–66

    Google Scholar 

  • Kagami M, Miki T, Takimoto G (2014) Mycoloop: chytrids in aquatic food webs. Front Microbiol 5:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanaya G, Solovyev MM, Shikano S, Okano J-I, Ponomareva NM, Yurlova NI (2019) Application of stable isotopic analyses for fish host-parasite systems: an evaluation tool for parasite-mediated material flow in aquatic ecosystems. Aquat Ecol 53:217–232

    Article  CAS  Google Scholar 

  • Kassambara A (2023) ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.6.0, https://rpkgs.datanovia.com/ggpubr/

  • Kennicutt MC, Chown SL, Cassano JJ, Liggett D, Peck LS, Massom R, Rintoul S, Storey J, Vaughan D, Wilson T (2015) A roadmap for Antarctic and Southern Ocean science for the next two decades and beyond. Antarct Sci 27:3–18

    Article  Google Scholar 

  • Kock K-H, Everson I (1997) Biology and ecology of mackerel icefish, Champsocephalus gunnari: an Antarctic fish lacking hemoglobin. Comp Biochem Physiol A Physiol 118:1067–1077

    Article  Google Scholar 

  • Kock K-H, Kellermann A (1991) Reproduction in Antarctic notothenioid fish. Antarct Sci 3:125–150

    Article  Google Scholar 

  • Kock K, Wilhelms S, Everson I, Groger J (1994) Variations in the diet composition and feeding intensity of mackerel icefish Champsocephalus gunnari at South Georgia (Antarctic). Mar Ecol Prog Ser 108:43–58

    Article  Google Scholar 

  • Kovaleva AA, Rodiuk GN, Grudnev MA (2002) Myxosporeans (Cnidospora: Myxosporea) of Antarctic fishes. Parazitologiia 36:502–513

    CAS  PubMed  Google Scholar 

  • Kuhn T, Zizka VMA, Muenster J, Klapper R, Mattiucci S, Kochmann J, Klimpel S (2018) Lighten up the dark: metazoan parasites as indicators for the ecology of Antarctic crocodile icefish (Channichthyidae) from the north-west Antarctic Peninsula. PeerJ 6:e4638

    Article  PubMed  PubMed Central  Google Scholar 

  • Kvach Y, Ondračková M, Bryjová A, Jurajda P (2017) Parasites as biological tags of divergence in central European gudgeon populations (Actinopterygii: Cyprinidae: Gobioninae). Biologia 72:671–679

    Article  Google Scholar 

  • Lea M-A, Nichols PD, Wilson G (2002) Fatty acid composition of lipid-rich myctophids and mackerel icefish (Champsocephalus gunnari)-Southern Ocean food-web implications. Polar Biol 25:843–854

    Article  Google Scholar 

  • Lönnberg E (1905) The fishes of the Swedish South Polar expedition. Lithographisches Institut des Generalstabs, Stockholm

    Google Scholar 

  • MacKenzie K, Campbell N, Mattiucci S, Ramos P, Pinto A, Abaunza P (2008) Parasites as biological tags for stock identification of Atlantic horse mackerel Trachurus trachurus L. Fish Res 89:136–145

    Article  Google Scholar 

  • MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:199–206

    Article  Google Scholar 

  • Marcogliese DJ (2003) Food webs and biodiversity: are parasites the missing link. J Parasitol 89:106–113

    Google Scholar 

  • Marcogliese DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1:151–164

    Article  Google Scholar 

  • Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35:705–716

    Article  PubMed  Google Scholar 

  • Munoz G, George-Nascimento M (2007) Two new species of Ascarophis (Nematoda: Cystidicolidae) in marine fishes from Chile. J Parasitol 93:1178–1188

    Article  PubMed  Google Scholar 

  • Nachev M, Jochmann MA, Walter F, Wolbert JB, Schulte SM, Schmidt TC, Sures B (2017) Understanding trophic interactions in host-parasite associations using stable isotopes of carbon and nitrogen. Parasit Vectors 10:1–9

    Article  Google Scholar 

  • Navarro J, Albo-Puigserver M, Coll M, Saez R, Forero MG, Kutcha R (2014) Isotopic discrimination of stable isotopes of nitrogen (δ15N) and carbon (δ13C) in a host-specific holocephalan tapeworm. J Helminthol 88:371–375

    Article  CAS  PubMed  Google Scholar 

  • Parker E, Jones CD, Arana PM, Alegría NA, Sarralde R, Gallardo F, Phillips AJ, Williams BW, Dornburg A (2020) Infestation dynamics between parasitic Antarctic fish leeches (Piscicolidae) and their crocodile icefish hosts (Channichthyidae). Polar Biol 43:665–677

    Article  Google Scholar 

  • Pasquaud S, Elie P, Jeantet C, Billy I, Martinez P, Girardin M (2008) A preliminary investigation of the fish food web in the Gironde estuary, France, using dietary and stable isotope analyses. Estuar Coast Shelf S 78:267–279

    Article  Google Scholar 

  • Patil I (2021) Visualizations with statistical details: the ‘ggstatsplot’ approach. J Open Source Softw 6:3167

    Article  Google Scholar 

  • Persson M, Larsson P, Stenroth P (2007) Fractionation of δ15N and δ13C for Atlantic salmon and its intestinal cestode Eubothrium crassum. J Fish Biol 71:441–452

    Article  CAS  Google Scholar 

  • Pinnegar J (2001) Unusual stable isotope fractionation patterns observed for fish host–parasite trophic relationships. J Fish Biol 59:494–503

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Power M, Klein GM (2004) Fish host-cestode parasite stable isotope enrichment patterns in marine, estuarine and freshwater fishes from northern Canada. Isotopes Environ Health Stud 40:257–266

    Article  CAS  PubMed  Google Scholar 

  • Quidor A (1906) Sur les copépodes recueillis par la mission Charcot dans les mers Antarctiques. Bulletin du Musée National d’Histoire Naturelle de Paris 12:27–33

    Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/

  • Reid K, Hill SL, Diniz TC, Collins MA (2005) Mackerel icefish Champsocephalus gunnari in the diet of upper trophic level predators at South Georgia: implications for fisheries management. Mar Ecol Prog Ser 305:153–161

    Article  Google Scholar 

  • Robinson SA, Forbes MR, Hebert CE (2010) Mercury in parasitic nematodes and trematodes and their double-crested cormorant hosts: bioaccumulation in the face of sequestration by nematodes. Sci Total Environ 408:5439–5444

    Article  CAS  PubMed  Google Scholar 

  • Rokicki J, Zdzitowiecki K (1991) Dynamics of Eubrachiella antarctica (Quidor, 1906) (Copepoda) occurrence in Notothenia rossii marmorata (Fischer, 1885). Acta Ichthyol Piscat 21:45–52

    Article  Google Scholar 

  • Ruhl HA, Hastings PA, Zarubick LA, Jensen RM, Zdzitowiecki K (2003) Fish populations of port foster, Deception Island, Antarctica and vicinity. Deep Sea Res. II Top Stud Oceanogr 50:1843–1858

    Article  Google Scholar 

  • Sabadel AJ, MacLeod CD (2022) Stable isotopes unravel the feeding mode-trophic position relationship in trematode parasites. J Anim Ecol 91:484–495

    Article  PubMed  Google Scholar 

  • Santoro M, Mattiucci S, Cipriani P, Bellisario B, Romanelli F, Cimmaruta R, Nascetti G (2014) Parasite communities of icefish (Chionodraco hamatus) in the Ross Sea (Antarctica): influence of the host sex on the helminth infracommunity structure. PLoS ONE 9:e88876

    Article  PubMed  PubMed Central  Google Scholar 

  • Siegel V (1980a) Parasite tags for some Antarctic channichthyid fish. Arch Fischereiwiss 31:97–103

    Google Scholar 

  • Siegel V (1980b) Quantitative investigations on parasites of Antarctic channichthyid and nototheniid fishes. Meeresforschung 28:146–156

    Google Scholar 

  • Sosinski J, Janusz J (1986) The occurrence of the parasite Eubrachiella gaini (Quidor, 1913) in Antarctic fishes of the family Chaenichthyidae. Acta Ichthyol Piscat 16:87–105

    Article  Google Scholar 

  • Sosinski J, Janusz J (2000) Infection variability of the parasitic copepod Eubrachiella antarctica (Quidor, 1906) on fishes in the Atlantic sector of the Antarctic. Bull Sea Fish Inst 2:25–42

    Google Scholar 

  • Sures B, Reimann N (2003) Analysis of trace metals in the Antarctic host-parasite system Notothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island. South Shetland Islands Polar Biol 26:680–686

    Article  Google Scholar 

  • Syväranta J, Lensu A, Marjomäki T, Oksanen S, Jones RI (2013) An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. PLoS ONE 8:e56094

    Article  PubMed  PubMed Central  Google Scholar 

  • Thieltges DW, Goedknegt MA, O’Dwyer K, Senior AM, Kamiya T (2019) Parasites and stable isotopes: a comparative analysis of isotopic discrimination in parasitic trophic interactions. Oikos 128:1329–1339

    Article  Google Scholar 

  • Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85

    Article  Google Scholar 

  • Timi JT, Poulin R (2020) Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 50:755–761

    Article  PubMed  Google Scholar 

  • Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158

    Article  Google Scholar 

  • Vander Zanden MJ, Shuter BJ, Lester NP, Rasmussen JB (2000) Within-and among-population variation in the trophic position of a pelagic predator, lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 57:725–731

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Wickham H, Averick M, Bryan J, Chang W, McGowan LDA, François R, Grolemund G, Hayes A, Henry L, Hester J (2019) Welcome to the tidyverse. J Open Source Softw 4:1686

    Article  Google Scholar 

  • Williams H, MacKenzie K, McCarthy A (1992) Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Rev Fish Biol Fisher 2:144–176

    Article  Google Scholar 

  • Zdzitowiecki K, Pisano E (1996) New records of Digenea infecting elasmobranch and teleost fish off Heard Island (Kerguelen sub-region, sub-Antarctic). J Appl Ichthyol 43:265–272

    Google Scholar 

Download references

Acknowledgements

The authors thank the Scientific Observers for krill fishery and the master and crew of the trawler Fuyuanyu 9818 for their considerable efforts to collect the samples. Haiting Zhang and Qingyuan Yang deserve special recognition for their contribution in the laboratory. The authors also thank the College of Marine Sciences, Shanghai Ocean University for providing the facilities in the laboratory that make this study happen. This project was supported by the International Science and Technology Cooperation Key Special Project of the National Key Research and Development Program (grant no 2023YFE0104500 to G.P. Zhu), and the National Science Foundation of China (grant 41776185 to G.P. Zhu).

Author information

Authors and Affiliations

  1. College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China

    Bixue Wang, Jing Ning & Guoping Zhu

  2. Center for Polar Research, Shanghai Ocean University, Shanghai, 201306, China

    Bixue Wang & Guoping Zhu

  3. Polar Marine Ecosystem Group, The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, Shanghai, 201306, China

    Guoping Zhu

  4. National Engineering Research Center for Oceanic Fisheries, Shanghai, 201306, China

    Guoping Zhu

Authors
  1. Bixue Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Ning
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guoping Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guoping Zhu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Handling editor: Rafael Leitão.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1916 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, B., Ning, J. & Zhu, G. Ectoparasite infestation and host–parasite trophic relationship for Champsocephalus gunnari (Lonnberg, 1905) at South Orkney Islands, Antarctica. Aquat Ecol (2023). https://doi.org/10.1007/s10452-023-10072-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10452-023-10072-4

Keywords

Search

Navigation