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Parasites as biological tags of fish stocks: a meta-analysis of their discriminatory power



The use of parasites as biological tags to discriminate among marine fish stocks has become a widely accepted method in fisheries management. Here, we first link this approach to its unstated ecological foundation, the decay in the similarity of the species composition of assemblages as a function of increasing distance between them, a phenomenon almost universal in nature. We explain how distance decay of similarity can influence the use of parasites as biological tags. Then, we perform a meta-analysis of 61 uses of parasites as tags of marine fish populations in multivariate discriminant analyses, obtained from 29 articles. Our main finding is that across all studies, the observed overall probability of correct classification of fish based on parasite data was about 71%. This corresponds to a two-fold improvement over the rate of correct classification expected by chance alone, and the average effect size (Zr = 0·463) computed from the original values was also indicative of a medium-to-large effect. However, none of the moderator variables included in the meta-analysis had a significant effect on the proportion of correct classification; these moderators included the total number of fish sampled, the number of parasite species used in the discriminant analysis, the number of localities from which fish were sampled, the minimum and maximum distance between any pair of sampling localities, etc. Therefore, there are no clear-cut situations in which the use of parasites as tags is more useful than others. Finally, we provide recommendations for the future usage of parasites as tags for stock discrimination, to ensure that future applications of the method achieve statistical rigour and a high discriminatory power.


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* Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand. Tel: +64 3 479-7983. Fax: +64 3 479-7584. E-mail:


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Arthur, J. R. and Albert, E. (1993). Use of parasites for separating stocks of Greenland halibut (Reinhardtius hippoglossoides) in the Canadian northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 50, 21752181. doi: 10.1139/f93-243.
Balbuena, J. and Raga, J. (1994). Intestinal helminths as indicators of segregation and social structure of pods of long-finned pilot whales (Globicephala melas) off the Faeroe Islands. Canadian Journal of Zoology 72, 443448.
Begg, C. B. and Mazumdar, M. (1994). Operating characteristics of a bank correlation test for publication bias. Biometrics 50, 10881101. doi: 10.2307/2533446.
Blaylock, R. B., Margolis, L. and Holmes, J. C. (2003). The use of parasites in discriminating stocks of Pacific halibut (Hippoglossus stenolepis) in the northeast Pacific. Fishery Bulletin 101, 19.
Boje, J., Riget, F. and Køie, M. (1997). Helminth parasites as biological tags in population studies of Greenland halibut (Reinhardtius hippoglossoides (Walbaum)), in the north-west Atlantic. ICES Journal of Marine Science 54, 886895. doi: 10.1006/jmsc.1997.0214.
Bradbury, I. R. and Bentzen, P. (2007). Non-linear genetic isolation by distance: implications for dispersal estimation in anadromous and marine fish populations. Marine Ecology Progress Series 340, 245257.
Braicovich, P. E., Luque, J. L. and Timi, J. T. (2012). Geographical patterns of parasite infracommunities in the rough scad, Trachurus lathami Nichols, in the southwestern Atlantic ocean. Journal of Parasitology 98, 768777. doi: 10.1645/ge-2950.1.
Braicovich, P. E. and Timi, J. T. (2008). Parasites as biological tags for stock discrimination of the Brazilian flathead Percophis brasiliensis in the south-west Atlantic. Journal of Fish Biology 73, 557571. doi: 10.1111/j.1095-8649.2008.01948.x.
Brickle, P. and MacKenzie, K. (2007). Parasites as biological tags for Eleginops maclovinus (Teleostei : Eleginopidae) around the Falkland Islands. Journal of Helminthology 81, 147153. doi: 10.1017/s0022149×07750514.
Cadrin, S. X. (2000). Advances in morphometric identification of fishery stocks. Reviews in Fish Biology and Fisheries 10, 91112.
Carballo, M. C., Cremonte, F., Navone, G. T. and Timi, J. T. (2012). Similarity in parasite community structure may be used to trace latitudinal migrations of Odontesthes smitti along Argentinean coasts. Journal of Fish Biology 80, 1528. doi: 10.1111/j.1095-8649.2011.03125.x.
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates Inc., Hillsdale, New Jersey.
Evans, D. and Grainger, R. (2002). Gathering data for resource monitoring and fisheries management. In Handbook of Fish Biology and Fisheries, Vol. 2 (ed. Hart, P. J. B. and Reynolds, J. D.), pp. 84102. Blackwell Publishing, Oxford.
Fellis, K. J. and Esch, G. W. (2005). Variation in life cycle affects the distance decay of similarity among bluegill sunfish parasite communities. Journal of Parasitology 91, 14841486.
Ferrer-Castello, 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, 169178. doi: 10.1017/s0022149×07729553.
Fox, J. and Weisberg, S. (2011). An R Companion to Applied Regression. Sage Publications, Thousand Oaks, California.
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33, 122.
Henriquez, V. P., González, M. T., Licandeo, R. and Carvajal, J. (2011). Metazoan parasite communities of rock cod Eleginops maclovinus along southern Chilean coast and their use as biological tags at a local spatial scale. Journal of Fish Biology 79, 18511865. doi: 10.1111/j.1095-8649.2011.03126.x.
Higgins, J. P. T., Thompson, S. G., Deeks, J. J. and Altman, D. G. (2003). Measuring inconsistency in meta-analyses. British Medical Journal 327, 557560. doi: 10.1136/bmj.327.7414.557.
Hilborn, R. and Walters, C. J. (1992). Quantitative Fisheries Stock Assessment: Choice, Dynamics and Uncertainty. Chapman and Hall, New York.
Hutson, K. S., Brock, E. L. and Steer, M. A. (2011). Spatial variation in parasite abundance: evidence of geographical population structuring in southern garfish Hyporhamphus melanochir . Journal of Fish Biology 78, 166182. doi: 10.1111/j.1095-8649.2010.02849.x.
Karvonen, A. and Valtonen, E. T. (2004). Helminth assemblages of whitefish (Coregonus lavaretus) in interconnected lakes: similarity as a function of species-specific parasites and geographical separation. Journal of Parasitology 90, 471476.
Krasnov, B. R., Shenbrot, G. I., Mouillot, D., Khokhlova, I. S. and Poulin, R. (2005). Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographic distance or faunal similarity? Journal of Biogeography 32, 633644.
Lester, R. J. G. and MacKenzie, K. (2009). The use and abuse of parasites as stock markers for fish. Fisheries Research 97, 12.
Lester, R. J. G., Sewell, K. B., Barnes, A. and Evans, K. (1988). Stock discrimination of orange roughy, Hoplostethus atlanticus, by parasite analysis. Marine Biology 99, 137143.
Li, B., Dettai, A., Cruaud, C., Couloux, A., Desoutter-Meniger, M. and Lecointre, G. (2009). RNF213, a new nuclear marker for acanthomorph phylogeny. Molecular Phylogenetics and Evolution 50, 345363. doi: 10.1016/j.ympev.2008.11.013.
Lipsey, M. W. and Wilson, D. B. (2001). Practical Meta-analysis. Sage Publications, Thousand Oaks, California.
Luque, J. L., Cordeiro, A. S. and Oliva, M. E. (2010). Metazoan parasites as biological tags for stock discrimination of whitemouth croaker Micropogonias furnieri . Journal of Fish Biology 76, 591600. doi: 10.1111/j.1095-8649.2009.02515.x.
MacKenzie, K. (2002). Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124, S153S163.
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, 4556.
Marques, J. F., Teixeira, C. M. and Cabral, H. N. (2006). Differentiation of commercially important flatfish populations along the Portuguese coast: evidence from morphology and parasitology. Fisheries Research 81, 293305. doi: 10.1016/j.fishres.2006.05.021.
Mattiucci, S. and Nascetti, G. (2008). Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes. Advances in Parasitology 66, 47148.
McClelland, G. and Melendy, J. (2007). Use of endoparasitic helminths as tags in delineating stocks of American plaice (Hippoglossoides platessoides) from the southern Gulf of St. Lawrence and Cape Breton Shelf. Fishery Bulletin 105, 180188.
McClelland, G. and Melendy, J. (2011). Use of parasites as tags in delineating stocks of Atlantic cod (Gadus morhua) from the southern Gulf of St. Lawrence and the Cape Breton Shelf. Fisheries Research 107, 233238. doi: 10.1016/j.fishres.2010.10.022.
McClelland, G., Melendy, J., Osborne, J., Reid, D. and Douglas, S. (2005). Use of parasite and genetic markers in delineating populations of winter flounder from the central and south-west Scotian Shelf and north-east Gulf of Maine. Journal of Fish Biology 66, 10821100. doi: 10.1111/j.1095-8649.2005.00659.x.
Melendy, J., McClelland, G. and Hurlbut, I. (2005). Use of parasite tags in delineating stocks of white hake (Urophycis tenuis) from the southern Gulf of St. Lawrence and Cape Breton Shelf. Fisheries Research 76, 392400. doi: 10.1016/j.fishres.2005.07.006.
Moore, B. R., Welch, D. J., Newman, S. J. and Lester, R. J. G. (2012). Parasites as indicators of movement and population connectivity of a non-diadromous, tropical estuarine teleost: king threadfin Polydactylus macrochir . Journal of Fish Biology 81, 230252. doi: 10.1111/j.1095-8649.2012.03335.x.
Morand, S. and Poulin, R. (2003). Phylogenies, the comparative method and parasite evolutionary ecology. Advances in Parasitology 54, 281302.
Morlon, H., Chuyong, G., Condit, R., Hubbell, S., Kenfack, D., Thomas, D., Valencia, R. and Green, J. L. (2008). A general framework for the distance-decay of similarity in ecological communities. Ecology Letters 11, 904917.
Mosquera, J., de Castro, M. and Gómez-Gesteira, M. (2003). Parasites as biological tags of fish populations: advantages and limitations. Comments on Theoretical Biology 8, 6991.
Nakagawa, S. and Cuthill, I. C. (2007). Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews 82, 591605. doi: 10.1111/j.1469-185X.2007.00027.x.
Nakagawa, S. and Santos, E. S. A. (2012). Methodological issues and advances in biological meta-analysis. Evolutionary Ecology 26, 12531274. doi: 10.1007/s10682-012-9555-5.
Nekola, J. C. and White, P. S. (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867878.
Niklitschek, E. J., Secor, D. H., Toledo, P., Lafon, A. and George-Nascimento, M. (2010). Segregation of SE Pacific and SW Atlantic southern blue whiting stocks: integrating evidence from complementary otolith microchemistry and parasite assemblage approaches. Environmental Biology of Fishes 89, 399413. doi: 10.1007/s10641-010-9695-9.
Oliva, M. E. and Ballon, I. (2002). Metazoan parasites of the Chilean hake Merluccius gayi gayi as a tool for stock discrimination. Fisheries Research 56, 313320. doi: 10.1016/s0165-7836(01)00329-0.
Oliva, M. E., Fernandez, I., Oyarzun, C. and Murillo, C. (2008). Metazoan parasites of the stomach of Dissostichus eleginoides Smitt 1898 (Pisces : Notothenidae) from southern Chile: a tool for stock discrimination? Fisheries Research 91, 119122. doi: 10.1016/j.fishres.2007.11.012.
Oliva, M. E. and González, M. T. (2005). The decay of similarity over geographical distance in parasite communities of marine fishes. Journal of Biogeography 32, 13271332.
Oliva, M. E. and Sánchez, M. F. (2005). Metazoan parasites and commensals of the northern Chilean scallop Argopecten purpuratus (Lamarck, 1819) as tools for stock identification. Fisheries Research 71, 7177.
Pérez-del-Olmo, A., Fernández, M., Raga, J. A., Kostadinova, A. and Morand, S. (2009). Not everything is everywhere: the distance decay of similarity in a marine host-parasite system. Journal of Biogeography 36, 200209.
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299.
Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 16091615.
Poulin, R. (2006). Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. International Journal for Parasitology 36, 877885.
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776.
Poulin, R., Blanar, C. A., Thieltges, D. W. and Marcogliese, D. J. (2011). The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34, 540551.
Poulin, R. and Forbes, M. R. (2012). Meta-analysis and research on host-parasite interactions: past and future. Evolutionary Ecology 26, 11691185.
Poulin, R. and Krasnov, B. R. (2010). Similarity and variability of parasite assemblages across geographical space. In The Biogeography of Host-Parasite Interactions (ed. Morand, S. and Krasnov, B. R.), pp. 115127. Oxford University Press, Oxford.
Poulin, R. and Leung, T. L. F. (2010). Taxonomic resolution in parasite community studies: are things getting worse? Parasitology 137, 19671973.
Poulin, R. and Morand, S. (1999). Geographic distances and the similarity among parasite communities of conspecific host populations. Parasitology 119, 369374.
Power, A. M., Balbuena, J. A. and Raga, J. A. (2005). Parasite infracommunities as predictors of harvest location of bogue (Boops boops L.): a pilot study using statistical classifiers. Fisheries Research 72, 229239. doi: 10.1016/j.fishres.2004.10.001.
R Development Core Team (2012). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Salinas, X., González, M. T. and Acuna, E. (2008). Metazoan parasites of the thumb grenadier Nezumia pulchella, from the south-eastern Pacific, off Chile, and their use for discrimination of host populations. Journal of Fish Biology 73, 683691. doi: 10.1111/j.1095-8649.2008.01967.x.
Sardella, N. H. and Timi, J. T. (2004). Parasites of Argentine hake in the Argentine Sea: population and infracommunity structure as evidence for host stock discrimination. Journal of Fish Biology 65, 14721488. doi: 10.1111/j.0022-1112.2004.00572.x.
Sequeira, V., Gordo, L. S., Neves, A., Paiva, R. B., Cabral, H. N. and Marques, J. F. (2010). Macroparasites as biological tags for stock identification of the bluemouth, Helicolenus dactylopterus (Delaroche, 1809) in Portuguese waters. Fisheries Research 106, 321328. doi: 10.1016/j.fishres.2010.08.014.
Soininen, J., McDonald, R. and Hillebrand, H. (2007). The distance decay of similarity in ecological communities. Ecography 30, 312.
Solow, A. (1990). A randomization test for misclassification probability in discriminant analysis. Ecology 71, 23792382.
Steinitz, O., Heller, J., Tsoar, A., Rotem, D. and Kadmon, R. (2006). Environment, dispersal and patterns of species similarity. Journal of Biogeography 33, 10441054.
Tabachnick, B. G. and Fidell, L. S. (2001). Using Multivariate Statistics. Allyn and Bacon, Boston.
Thieltges, D. W., Dolch, T., Krakau, M. and Poulin, R. (2010). Salinity gradient shapes distance decay of similarity among parasite communities in three marine fishes. Journal of Fish Biology 76, 18061814.
Thieltges, D. W., Ferguson, M. A. D., Jones, C. S., Krakau, M., de Montaudouin, X., Noble, L. R., Reise, K. and Poulin, R. (2009). Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160, 163173.
Timi, J. T. and Lanfranchi, A. L. (2009). The metazoan parasite communities of the Argentinean sandperch Pseudopercis semifasciata (Pisces: Perciformes) and their use to elucidate the stock structure of the host. Parasitology 136, 12091219. doi: 10.1017/s0031182009990503.
Timi, J. T., Lanfranchi, A. L. and Etchegoin, J. A. (2009). Seasonal stability and spatial variability of parasites in Brazilian sandperch Pinguipes brasilianus from the Northern Argentine Sea: evidence for stock discrimination. Journal of Fish Biology 74, 12061225. doi: 10.1111/j.1095-8649.2009.02190.x.
Timi, J. T., Lanfranchi, A. L., Etchegoin, J. A. and Cremonte, F. (2008). Parasites of the Brazilian sandperch Pinguipes brasilianus Cuvier: a tool for stock discrimination in the Argentine Sea. Journal of Fish Biology 72, 13321342. doi: 10.1111/j.1095-8649.2008.01800.x.
Timi, J. T., Lanfranchi, A. L. and Luque, J. L. (2010). Similarity in parasite communities of the teleost fish Pinguipes brasilianus in the southwestern Atlantic: infracommunities as a tool to detect geographical patterns. International Journal for Parasitology 40, 243254.
Timi, J. T., Luque, J. L. and Sardella, N. H. (2005). Parasites of Cynoscion guatucupa along South American Atlantic coasts: evidence for stock discrimination. Journal of Fish Biology 67, 16031618. doi: 10.1111/j.1095-8649.2005.00867.x.
Titus, K., Mosher, J. A. and Williams, B. K. (1984). Chance-corrected classification for use in discriminant analysis: ecological applications. American Midland Naturalist 111, 17.
Vales, D. G., Garciá, N. A., Crespo, E. A. and Timi, J. T. (2011). Parasites of a marine benthic fish in the Southwestern Atlantic: searching for geographical recurrent patterns of community structure. Parasitology Research 108, 261272.
Varela, A. I., Ritchie, P. A. and Smith, P. J. (2012). Low levels of global genetic differentiation and population expansion in the deep-sea teleost Hoplostethus atlanticus revealed by mitochondrial DNA sequences. Marine Biology 159, 10491060.
Varela, A. I., Ritchie, P. A. and Smith, P. J. (2013). Global genetic population structure in the commercially exploited deep-sea teleost orange roughy (Hoplostethus atlanticus) based on microsatellite DNA analysis. Fisheries Research 140, 8390.
Williams, H. H., MacKenzie, K. and McCarthy, A. M. (1992). Parasites as biological indicators of the population biology, migrations, diet and phylogenetics of fish. Reviews in Fish Biology and Fisheries 2, 144176.
Yamaguchi, A., Yokoyama, H., Ogawa, K. and Taniuchi, T. (2003). Use of parasites as biological tags for separating stocks of the starspotted dogfish Mustelus manazo in Japan and Taiwan. Fisheries Science 69, 337342. doi: 10.1046/j.1444-2906.2003.00626.x.


Parasites as biological tags of fish stocks: a meta-analysis of their discriminatory power



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