Skip to main content Accessibility help
×
×
Home

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

  • ALYSSA R. CIRTWILL (a1), DANIEL B. STOUFFER (a1), ROBERT POULIN (a2) and CLÉMENT LAGRUE (a2)

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.

Copyright

Corresponding author

* 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

References

Hide All
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, 16251632.
Araujo, M. S., Bolnick, D. I. and Layman, C. A. (2011). The ecological causes of individual specialisation. Ecology Letters 14, 948958.
Barton, K. (2014). Package ‘MuMIn’: multi-model inference. R package Version 1.9. 13.
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.
Bell, G. and Burt, A. (1991). The comparative biology of parasite species diversity: internal helminths of freshwater fish. Journal of Animal Ecology 60, 10471064.
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, 555572.
Bolnick, D. I., Yang, L. H., Fordyce, J. A., Davis, J. M. and Svanback, R. (2002). Measuring individual-level resource specialization. Ecology 83, 29362941.
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, 128.
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, 24782485.
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, 785795.
Carney, J. P. and Dick, T. A. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538555.
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179193.
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, 186194.
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, 297304.
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, 459477.
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, 7587.
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, 13691377.
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33, 122. http://www.jstatsoft.org/v33/i02/.
Hubert, W. A. (1996). Passive capture techniques. In Fisheries Techniques, 2nd Edn (ed. Murphy, B. R. and Willis, D. W.), pp. 157192. American Fisheries Society, Bethesda, MD, USA.
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, 585598.
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, 12911301.
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, 379388.
Kennedy, C. R., Bush, A. O. and Aho, J. M. (1986). Patterns in helminth communities: why are birds and fish different? Parasitology 93, 205215.
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, 249257.
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, 20032009.
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, 847859.
Knudsen, R., Curtis, M. A. and Kristofferson, R. (2004). Aggregation of helminths: the role of feeding behaviour of fish hosts. Journal of Parasitology 90, 17.
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, 107116.
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, 12291246.
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.
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, 466485.
Layman, C. A., Newsome, S. D. and Crawford, T. G. (2015). Individual-level niche specialization within populations: emerging areas of study. Oecologia 178, 14.
Lile, N. K. (1998). Alimentary tract helminths of four pleuronectid flatfish in relation to host phylogeny and ecology. Journal of Fish Biology 53, 945953.
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, 16951708.
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, 7383.
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, 253262.
Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology 124, S83S99.
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, 151164.
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, 107121.
McDowall, R. M. (1990). New Zealand Freshwater Fishes: A Natural History and Guide. Heinemann Reed/MAF Publishing Group, Auckland, New Zealand.
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, 6573.
Nielsen, L. A. and Johnson, D. L. (1983). Fisheries Techniques. American Fisheries Society, Bethesda, MD, USA.
Novak, M. and Tinker, M. T. (2015). Timescales alter the inferred strength and temporal consistency of intraspecific diet specialization. Oecologia 178, 6174.
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature 425, 480484.
Poulin, R. (1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283302.
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, 123137.
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776.
Poulin, R. (2013). Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541546.
Poulin, R. and Leung, T. L. F. (2011). Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166, 731738.
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, 12351243.
R Development Core Team (2014). R: A Language Environment for Statistical Computing. Vienna, Austria. http://www.R-project.org
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, 516.
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, 511525.
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, 103114.
Valtonen, E. T., Marcogliese, D. J. and Julkunen, M. (2010). Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay. Oecologia 162, 139152.
Wainwright, P. C. and Richard, B. A. (1995). Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fishes 44, 97113.
Wilson, D. S., Muzzall, P. M. and Ehlinger, J. (1996). Parasites, morphology, and habitat use in a bluegill sunfish (Lepomis macrochirus) population. Copeia 2, 348354.
Zelmer, D. A. (2014). Size, time, and asynchrony matter: the species-area relationship for parasites of freshwater fishes. Journal of Parasitology 100, 561568.
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, 2428.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Cirtwill supplementary material
Cirtwill supplementary material 1

 Word (5.6 MB)
5.6 MB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed