Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-25T15:43:33.115Z Has data issue: false hasContentIssue false
  • English
  • Français

Are parasite richness and abundance linked to prey species richness and individual feeding preferences in fish hosts?

Published online by Cambridge University Press:  17 November 2015

ALYSSA R. CIRTWILL ,
DANIEL B. STOUFFER ,
ROBERT POULIN  and
CLÉMENT LAGRUE
ALYSSA R. CIRTWILL
Affiliation:
Centre for Integrative Ecology, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand
DANIEL B. STOUFFER
Affiliation:
Centre for Integrative Ecology, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, 340 Great King Street, PO Box 56, Dunedin 9054, New Zealand
CLÉMENT LAGRUE*
Affiliation:
Department of Zoology, University of Otago, 340 Great King Street, PO Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, 340 Great King Street, PO Box 56, Dunedin 9054, New Zealand. E-mail: clement.lagrue@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Variations in levels of parasitism among individuals in a population of hosts underpin the importance of parasites as an evolutionary or ecological force. Factors influencing parasite richness (number of parasite species) and load (abundance and biomass) at the individual host level ultimately form the basis of parasite infection patterns. In fish, diet range (number of prey taxa consumed) and prey selectivity (proportion of a particular prey taxon in the diet) have been shown to influence parasite infection levels. However, fish diet is most often characterized at the species or fish population level, thus ignoring variation among conspecific individuals and its potential effects on infection patterns among individuals. Here, we examined parasite infections and stomach contents of New Zealand freshwater fish at the individual level. We tested for potential links between the richness, abundance and biomass of helminth parasites and the diet range and prey selectivity of individual fish hosts. There was no obvious link between individual fish host diet and helminth infection levels. Our results were consistent across multiple fish host and parasite species and contrast with those of earlier studies in which fish diet and parasite infection were linked, hinting at a true disconnect between host diet and measures of parasite infections in our study systems. This absence of relationship between host diet and infection levels may be due to the relatively low richness of freshwater helminth parasites in New Zealand and high host–parasite specificity.

Keywords

fish diethelminth parasitesinfection levelsindividual hosttransmission mode
Type
Research Article
Information
Parasitology , Volume 143 , Issue 1 , January 2016 , pp. 75 - 86
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albon, S. D., Stien, A., Irvine, R. J., Langvatn, R., Ropstad, E. and Halvorsen, O. (2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London B 269, 1625–1632.CrossRefGoogle ScholarPubMed
Araujo, M. S., Bolnick, D. I. and Layman, C. A. (2011). The ecological causes of individual specialisation. Ecology Letters 14, 948–958.CrossRefGoogle ScholarPubMed
Barton, K. (2014). Package ‘MuMIn’: multi-model inference. R package Version 1.9. 13.Google Scholar
Bates, D., Mächler, M., Bolker, B. and Walker, S. (2014). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, arXiv preprint arXiv:1406.5823.Google Scholar
Bell, G. and Burt, A. (1991). The comparative biology of parasite species diversity: internal helminths of freshwater fish. Journal of Animal Ecology 60, 1047–1064.CrossRefGoogle Scholar
Bertrand, M., Marcogliese, D. J. and Magnan, P. (2008). Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. Journal of Fish Biology 72, 555–572.CrossRefGoogle Scholar
Bolnick, D. I., Yang, L. H., Fordyce, J. A., Davis, J. M. and Svanback, R. (2002). Measuring individual-level resource specialization. Ecology 83, 2936–2941.CrossRefGoogle Scholar
Bolnick, D. I., Svanback, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D. and Forister, M. L. (2003). The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161, 1–28.CrossRefGoogle ScholarPubMed
Bouillon, D. R. and Dempson, J. B. (1989). Metazoan parasite infections in landlocked and anadromous Arctic charr (Salvelinus alpinus Linnaeus), and their use as indicators of movement to sea in young anadromous charr. Canadian Journal of Zoology 67, 2478–2485.CrossRefGoogle Scholar
Carney, J. P. and Dick, T. A. (1999). Enteric helminths of perch (Perca fluviatilis L.) and yellow perch (Perca flavescens Mitchill): stochastic or predictable assemblages? Journal of Parasitology 5, 785–795.CrossRefGoogle Scholar
Carney, J. P. and Dick, T. A. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538–555.CrossRefGoogle Scholar
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
Curtis, M. A., Berube, M. and Stenzel, A. (1995). Parasitological evidence for specialized foraging behaviour in lake-resident Arctic char (Salvelinus alpinus). Canadian Journal of Fisheries and Aquatic Sciences 52, 186–194.CrossRefGoogle Scholar
Dick, T., Chamber, C. and Gallagher, C. P. (2009). Parasites, diet and stable isotopes of shorthorn sculpin (Myoxocephalus scorpius) from Frobisher Bay, Canada. Parasite 16, 297–304.CrossRefGoogle ScholarPubMed
Ebert, D., Lipsitch, M. and Mangin, K. L. (2000). The effects of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. American Naturalist 156, 459–477.CrossRefGoogle ScholarPubMed
Fodrie, F. J., Yeager, L. A., Grabowski, J. H., Layman, C. A., Sherwood, G. D. and Kenworthy, M. D. (2015). Measuring individuality in habitat use across complex landscapes: approaches, constraints, and implications for assessing resource specialization. Oecologia 178, 75–87.CrossRefGoogle ScholarPubMed
Gonzalez, M. T. and Poulin, R. (2005). Spatial and temporal predictability of the parasite community structure of a benthic marine fish along its distributional range. International Journal for Parasitology 35, 1369–1377.CrossRefGoogle ScholarPubMed
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33, 1–22. http://www.jstatsoft.org/v33/i02/.CrossRefGoogle Scholar
Hubert, W. A. (1996). Passive capture techniques. In Fisheries Techniques, 2nd Edn (ed. Murphy, B. R. and Willis, D. W.), pp. 157–192. American Fisheries Society, Bethesda, MD, USA.Google Scholar
Hyndes, G. A., Platell, M. E. and Potter, I. C. (1997). Relationships between diet and body size, mouth morphology, habitat and movements of six sillaginid species in coastal waters: implications for resource partitioning. Marine Biology 128, 585–598.CrossRefGoogle Scholar
Johnson, M. W., Nelson, P. A. and Dick, T. A. (2004 a). Structuring mechanisms of yellow perch (Perca flavescens) parasite communities: host age, diet, and local factors. Canadian Journal of Zoology 82, 1291–1301.CrossRefGoogle Scholar
Johnson, M. W., Hesslein, R. H. and Dick, T. A. (2004 b). Host length, age, diet, parasites and stable isotopes as predictors of yellow perch (Perca flavescens Mitchill), trophic status in nutrient poor Canadian Shield lakes. Environmental Biology of Fishes 71, 379–388.CrossRefGoogle Scholar
Kennedy, C. R., Bush, A. O. and Aho, J. M. (1986). Patterns in helminth communities: why are birds and fish different? Parasitology 93, 205–215.CrossRefGoogle ScholarPubMed
Klimpel, S., Ruckert, S., Piatkowski, U., Palm, H. W. and Hanel, R. (2006). Diet and metazoan parasites of silver scabbard fish Lepidopus caudatus from the Great Meteor Seamount (North Atlantic). Marine Ecology Progress Series 315, 249–257.CrossRefGoogle Scholar
Knudsen, R., Kristoffersen, R. and Amundsen, P.-A. (1997). Parasite communities in two sympatric morphs of Arctic charr, Salvelinus alpinus (L.), in northern Norway. Canadian Journal of Zoology 75, 2003–2009.CrossRefGoogle Scholar
Knudsen, R., Amundsen, P.-A. and Klementsen, A. (2003). Inter- and intra-morph patterns in helminth communities of sympatric whitefish morphs. Journal of Fish Biology 62, 847–859.CrossRefGoogle Scholar
Knudsen, R., Curtis, M. A. and Kristofferson, R. (2004). Aggregation of helminths: the role of feeding behaviour of fish hosts. Journal of Parasitology 90, 1–7.CrossRefGoogle ScholarPubMed
Knudsen, R., Amundsen, P.-A., Nilsen, R., Kristofferson, R. and Klementsen, A. (2008). Food borne parasites as indicators of trophic segregation between Arctic charr and brown trout. Environmental Biology of Fishes 83, 107–116.CrossRefGoogle Scholar
Kristoffersen, K., Halvorsen, M. and Jørgensen, L. (1994). Influence of parr growth, lake morphology, and freshwater parasites on the degree of anadromy in different populations of Arctic char (Salvelinus alpinus) in northern Norway. Canadian Journal of Fisheries and Aquatic Sciences 51, 1229–1246.CrossRefGoogle Scholar
Kuznetsova, A., Brockhoff, P. B. and Christensen, R. H. B. (2014). Package “lmerTest”: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R Package Version 2.0–3.Google Scholar
Lagrue, C., Kelly, D. W., Hicks, A. and Poulin, R. (2011). Factors influencing infection patterns of trophically transmitted parasites among a fish community: host diet, host-parasite compatibility or both? Journal of Fish Biology 79, 466–485.Google ScholarPubMed
Layman, C. A., Newsome, S. D. and Crawford, T. G. (2015). Individual-level niche specialization within populations: emerging areas of study. Oecologia 178, 1–4.CrossRefGoogle ScholarPubMed
Lile, N. K. (1998). Alimentary tract helminths of four pleuronectid flatfish in relation to host phylogeny and ecology. Journal of Fish Biology 53, 945–953.CrossRefGoogle Scholar
Lo, C., Morand, S. and Galzin, R. (1998). Parasite diversity/host age and size relationship in three coral-reef fishes from French Polynesia. International Journal for Parasitology 28, 1695–1708.CrossRefGoogle ScholarPubMed
Locke, S. A., McLaughlin, J. D. and Marcogliese, D. J. (2013). Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122, 73–83.CrossRefGoogle Scholar
Locke, S. A., Marcogliese, D. J. and Valtonen, E. T. (2014). Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia 174, 253–262.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology 124, S83–S99.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, 151–164.CrossRefGoogle Scholar
Marques, J. F., Santos, M. J., Teixeira, C. M., Batista, M. I. and Cabral, H. N. (2011). Host-parasite relationship in flatfish (Pleuronectiformes) – the relative importance of host biology, ecology and phylogeny. Parasitology 138, 107–121.CrossRefGoogle Scholar
McDowall, R. M. (1990). New Zealand Freshwater Fishes: A Natural History and Guide. Heinemann Reed/MAF Publishing Group, Auckland, New Zealand.Google Scholar
Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., Faliex, E., Galzin, R., Lo, C. M., Lo-Yat, A., Pichelin, S. and Sasal, P. (2000). Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology 121, 65–73.CrossRefGoogle ScholarPubMed
Nielsen, L. A. and Johnson, D. L. (1983). Fisheries Techniques. American Fisheries Society, Bethesda, MD, USA.Google Scholar
Novak, M. and Tinker, M. T. (2015). Timescales alter the inferred strength and temporal consistency of intraspecific diet specialization. Oecologia 178, 61–74.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature 425, 480–484.CrossRefGoogle ScholarPubMed
Poulin, R. (1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283–302.CrossRefGoogle Scholar
Poulin, R. (2000). Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology 56, 123–137.CrossRefGoogle Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763–776.CrossRefGoogle ScholarPubMed
Poulin, R. (2013). Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541–546.CrossRefGoogle ScholarPubMed
Poulin, R. and Leung, T. L. F. (2011). Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166, 731–738.CrossRefGoogle ScholarPubMed
Poulin, R. and Valtonen, E. T. (2002). The predictability of helminth community structure in space: a comparison of fish populations from adjacent lakes. International Journal for Parasitology 32, 1235–1243.CrossRefGoogle ScholarPubMed
R Development Core Team (2014). R: A Language Environment for Statistical Computing. Vienna, Austria. http://www.R-project.org Google Scholar
Rosenblatt, A. E., Nifong, J. C., Heithaus, M. R., Mazzoti, F. J., Cherkiss, M. S., Jeffery, B. M., Elsey, R. M., Decker, R. A., Silliman, B. R., Guillette, L. J. Jr., Lowers, R. H. and Larson, J. C. (2015). Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178, 5–16.CrossRefGoogle ScholarPubMed
Simkova, A., Morand, S., Matejusova, I., Jurajda, P. and Gelnar, M. (2001). Local and regional influences on patterns of parasite species richness of central European fishes. Biodiversity and Conservation 10, 511–525.CrossRefGoogle Scholar
Svanback, R., Quevedo, M., Olsson, J. and Eklov, P. (2015). Individuals in food webs: the relationships between trophic position, omnivory and among-individual diet variation. Oecologia 178, 103–114.CrossRefGoogle ScholarPubMed
Valtonen, E. T., Marcogliese, D. J. and Julkunen, M. (2010). Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162, 139–152.CrossRefGoogle ScholarPubMed
Wainwright, P. C. and Richard, B. A. (1995). Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fishes 44, 97–113.CrossRefGoogle Scholar
Wilson, D. S., Muzzall, P. M. and Ehlinger, J. (1996). Parasites, morphology, and habitat use in a bluegill sunfish (Lepomis macrochirus) population. Copeia 2, 348–354.CrossRefGoogle Scholar
Zelmer, D. A. (2014). Size, time, and asynchrony matter: the species-area relationship for parasites of freshwater fishes. Journal of Parasitology 100, 561–568.CrossRefGoogle ScholarPubMed
Zelmer, D. A. and Arai, H. P. (1998). The contributions of host age and size to aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta. Canadian Journal of Parasitology 84, 24–28.CrossRefGoogle ScholarPubMed
Supplementary material: File

Cirtwill supplementary material

Cirtwill supplementary material 1

Download Cirtwill supplementary material(File)
File 5.6 MB