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The monogenean Paradiplozoon ichthyoxanthon behaves like a micropredator on two of its hosts, as indicated by stable isotopes

Published online by Cambridge University Press:  22 May 2018

B. Sures
Affiliation:
Aquatic Ecology, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany Centre for Water and Environmental Research, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa
M. Nachev
Affiliation:
Aquatic Ecology, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany Centre for Water and Environmental Research, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany
B.M. Gilbert
Affiliation:
Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa
Q.M. Dos Santos
Affiliation:
Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa
M.A. Jochmann
Affiliation:
Centre for Water and Environmental Research, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany Instrumental Analytical Chemistry, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany
D. Köster
Affiliation:
Instrumental Analytical Chemistry, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany
T.C. Schmidt
Affiliation:
Centre for Water and Environmental Research, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany Instrumental Analytical Chemistry, University of Duisburg-Essen, Universitätsstr. 5, 45141 Essen, Germany
A. Avenant-Oldewage
Affiliation:
Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa
Corresponding
E-mail address:

Abstract

The analysis of stable isotopes of carbon and nitrogen has been used as a fingerprint for understanding the trophic interactions of organisms. Most of these studies have been applied to free-living organisms, while parasites have largely been neglected. Studies dealing with parasites so far have assessed the carbon and nitrogen signatures in endoparasites or ectoparasites of different hosts, without showing general trends concerning the nutritional relationships within host–parasite associations. Moreover, in most cases such systems involved a single host and parasite species. The present study is therefore the first to detail the trophic interactions of a freshwater monogenean–host model using δ13C and δ15N, where a single monogenean species infects two distinctly different hosts. Host fishes, Labeobarbus aeneus and Labeobarbus kimberleyensis from the Vaal Dam, South Africa, were assessed for the monogenean parasite Paradiplozoon ichthyoxanthon, individuals of which were removed from the gills of the hosts. The parasites and host muscle samples were analysed for signatures of δ13C and δ15N using an elemental analyser connected to an isotope ratio mass spectrometer. Host fish appear to use partly different food sources, with L. aeneus having slightly elevated δ13C signatures compared to L. kimberleyensis, and showed only small differences with regard to their nitrogen signatures, suggesting that both species range on the same trophic level. Carbon and nitrogen signatures in P. ichthyoxanthon showed that the parasites mirrored the small differences in dietary carbon sources of the host but, according to δ15N signatures, the parasite ranged on a higher trophic level than the hosts. This relationship resembles predator–prey relationships and therefore suggests that P. ichthyoxanthon might act as a micropredator, similar to blood-sucking arthropods such as mites and fleas.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Avenant-Oldewage, A and Milne, SJ (2014) Aspects of the morphology of the juvenile life stages of Paradiplozoon ichthyoxanthon Avenant-Oldewage, 2013 (Monogenea: Diplozoidae). Acta Parasitologica 59, 247254.CrossRefGoogle Scholar
Avenant-Oldewage, A, Le Roux, LE, Mashego, SN and Jansen Van Vuuren, B (2014) Paradiplozoon ichthyoxanthon n. sp. (Monogenea: Diplozoidae) from Labeobarbus aeneus (Cyprinidae) in the Vaal River, South Africa. Journal of Helminthology 88, 166172.CrossRefGoogle ScholarPubMed
Barrett, J (1981) Biochemistry of parasitic helminths. London, Macmillan.CrossRefGoogle Scholar
Behrmann-Godel, J and Yohannes, E (2013) Multiple isotope analyses of the pike tapeworm Triaenophorus nadulosus reveal peculiarities in consumer-diet discrimination patterns. Journal of Helminthology 89, 238243.CrossRefGoogle Scholar
Boag, B, Neilson, R, Robinson, D, Scrimgeour, CM and Handley, LL (1998) Wild rabbit host and some parasites show trophic-level relationships for δ 13C and δ 15N: A first report. Isotopes in Environmental and Health Studies 34, 8185.CrossRefGoogle Scholar
Deudero, S, Pinnegar, JK and Polunin, NVC (2002) Insights into fish host–parasite trophic relationships revealed by stable isotope analysis. Diseases of Aquatic Organisms 52, 7786.CrossRefGoogle ScholarPubMed
Doi, H, Yurlova, NI, Vodyanitskaya, SN, Kanaya, G, Shikano, S and Kikuchi, E (2010) Estimating isotope fractionation between cercariae and host snail with the use of isotope measurement designed for very small organisms. Journal of Parasitology 96, 314317.CrossRefGoogle ScholarPubMed
Doucett, RR, Giberson, DJ and Power, G (1999) Parasitic association of Nanocladius (Diptera: Chironomidae) and Pteronarcys biloba (Plecoptera: Pteronarcyidae): insights from stable-isotope analysis. Journal of the North American Benthological Society 18, 514523.CrossRefGoogle Scholar
Dubois, SY, Savoye, N, Sauriau, PG, Billy, I, Martinez, P and de Montaudouin, X (2009) Digenean trematodes–marine mollusc relationships: a stable isotope study. Diseases of Aquatic Organisms 84, 6577.CrossRefGoogle ScholarPubMed
Fry, B (2006) Stable isotope ecology, New York, Springer-Verlag.CrossRefGoogle Scholar
Heincke, F (1908) Bericht über die Untersuchungen der Biologischen Anstalt auf Helgoland zur Naturgeschichte der Nutzfische. Die Beteiligung Deutschlands an der Internationalen Meeresforschung 1908 4/5, 67155.Google Scholar
Ikken, K, Brey, T, Wand, U, Voigt, J and Junghans, P (2001) Food web structure of the benthic community at the Procupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Progress in Oceanography 50, 383405.CrossRefGoogle Scholar
Le Brun, N, Renaud, F and Lambert, A (1988) The genus Diplozoon (Monogenea, Polyopisthocotylea) in Southern France; speciation and specificity. International Journal for Parasitology 18, 395400.CrossRefGoogle Scholar
McGrew, AK, O'Hara, TM, Stricker, CA, Castellini, JM, Beckmen, KB, Salman, MD and Ballweber, LR (2015) Ecotoxicoparasitology: understanding mercury concentrations in gut contents, intestinal helminths and host tissues of Alaskan gray wolves. Science of the Total Environment 536, 866871.CrossRefGoogle ScholarPubMed
Minagawa, M and Wada, E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ 15N and animal age. Geochimica Cosmochimica Acta 48, 11351140.CrossRefGoogle Scholar
Nachev, M, Jochmann, MA, Walter, F, Wolbert, JB, Schulte, SM, Schmidt, TC and Sures, B (2017) Understanding trophic interactions in host–parasite associations using stable isotopes of carbon and nitrogen. Parasites & Vectors 10, 90.CrossRefGoogle ScholarPubMed
Nash, RDM, Valencia, AH and Geffen, AJ (2006) The origin of Fulton's condition factor – setting the record straight. Fisheries 31, 236238.Google Scholar
Navarro, J, Albo-Puigserver, M, Coll, M, Saet, R, Forero, MG and Kutcha, R (2014) Isotopic discrimination of stable isotopes of nitrogen (δ 15N) and carbon (δ 13C) in a host-specific holocephalan tapeworm. Journal of Helminthology 88, 371375.CrossRefGoogle Scholar
Neilson, R, Boag, B and Hartley, G (2005) Temporal host–parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.) as revealed by stable isotope analyses. Parasitology 131, 279285.CrossRefGoogle ScholarPubMed
O'Grady, SP and Dearing, MD (2006) Isotopic insight into host–endosymbiont relationships in Liolaemid lizards. Oecologia 150, 355361.CrossRefGoogle ScholarPubMed
Persson, ME, Larsson, P and Stenroth, P (2007) Fractioning of δ 15N and δ 13C for Atlantic salmon and its intestinal cestode Eubothrium crissum. Journal of Fish Biology 71, 441452.CrossRefGoogle Scholar
Pinnegar, JK, Campbell, N and Polunin, NVC (2001) Unusual stable isotope fractionation patterns observed for fish–parasite trophic relationship. Journal of Fish Biology 59, 494503.Google Scholar
Post, DM, Pace, ML and Hairston, NG Jr (2000) Ecosystem size determines food-chain length in lakes. Nature 405, 10471049.CrossRefGoogle ScholarPubMed
Power, M and Klein, GM (2004) Fish host–cestode parasite stable isotope enrichment patterns in marine, estuarine and freshwater fishes from northern Canada. Isotopes in Environmental and Health Studies 40, 257266.CrossRefGoogle ScholarPubMed
Rhode, K (1993) Ecology of marine parasites. Wallingford, UK, CAB International.Google Scholar
Sabadel, AJM, Woodward, EMS, Van Hale, R and Frew, RD (2016) Compound-specific isotope analysis of amino acids: a tool to unravel complex symbiotic trophic relationships. Food Webs 6, 918.CrossRefGoogle Scholar
Schmidt, O, Dautel, H, Newton, J and Gray, JS (2011) Natural isotope signatures of host blood are replicated in moulted ticks. Ticks and Tick-borne Diseases 2, 225227.CrossRefGoogle ScholarPubMed
Skelton, P (2001) Freshwater fishes of Southern Africa. Cape Town, Struik Publishers.Google Scholar
Vander Zanden, M, Cabana, G and Rasmussen, J (1997) Comparing the trophic position of littoral fish estimated using stable nitrogen isotopes (δ 15N) and dietary data. Canadian Journal of Fisheries and Aquatic Sciences 54, 11421158.CrossRefGoogle Scholar
Voigt, CC and Kelm, DH (2006) Host preferences of bat flies: following the bloody path of stable isotopes in a host–parasite food chain. Canadian Journal of Zoology 84, 397403.CrossRefGoogle Scholar
Wada, E (2009) Stable δ 15N and δ 13C isotope ratios in aquatic ecosystems. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences 85, 98107.Google Scholar
Werner, RA and Brand, WA (2001) Referencing strategies and techniques in stable isotope ratio analysis. Rapid Communications in Mass Spectrometry 15, 501519.CrossRefGoogle ScholarPubMed
Yohannes, E, Grimm, C, Rothhaupt, KO and Behrmann-Godel, J (2017) The effect of parasite infection on stable isotope turnover rates of δ 15N, δ 13C and δ 34S in multiple tissues of Eurasian perch Perca fluviatilis. PLOS One 12, e0169058.CrossRefGoogle ScholarPubMed

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The monogenean Paradiplozoon ichthyoxanthon behaves like a micropredator on two of its hosts, as indicated by stable isotopes
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