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Mutual dilution of infection by an introduced parasite in native and invasive stream fishes across Hawaii

Published online by Cambridge University Press:  11 July 2016

RODERICK B. GAGNE ,
DAVID C. HEINS ,
PETER B. MCINTYRE ,
JAMES F. GILLIAM  and
MICHAEL J. BLUM
RODERICK B. GAGNE*
Affiliation:
Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA
DAVID C. HEINS
Affiliation:
Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA
PETER B. MCINTYRE
Affiliation:
Center for Limnology, University of Wisconsin, Madison, WI 53706, USA
JAMES F. GILLIAM
Affiliation:
Department of Biology, North Carolina State University, Raleigh, NC 27695, USA
MICHAEL J. BLUM
Affiliation:
Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA Tulane-Xavier Center for Bioenvironmental Research, Tulane University, 627 Lindy Boggs, New Orleans, LA 70118, USA
*
*Corresponding author. University of Wyoming, 1174 Snowy Range Rd. Laramie, WY 82070, USA. E-mail: [email protected]
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Summary

The presence of introduced hosts can increase or decrease infections of co-introduced parasites in native species of conservation concern. In this study, we compared parasite abundance, intensity, and prevalence between native Awaous stamineus and introduced poeciliid fishes by a co-introduced nematode parasite (Camallanus cotti) in 42 watersheds across the Hawaiian Islands. We found that parasite abundance, intensity and prevalence were greater in native than introduced hosts. Parasite abundance, intensity and prevalence within A. stamineus varied between years, which largely reflected a transient spike in infection in three remote watersheds on Molokai. At each site we measured host factors (length, density of native host, density of introduced host) and environmental factors (per cent agricultural and urban land use, water chemistry, watershed area and precipitation) hypothesized to influence C. cotti abundance, intensity and prevalence. Factors associated with parasitism differed between native and introduced hosts. Notably, parasitism of native hosts was higher in streams with lower water quality, whereas parasitism of introduced hosts was lower in streams with lower water quality. We also found that parasite burdens were lower in both native and introduced hosts when coincident. Evidence of a mutual dilution effect indicates that introduced hosts can ameliorate parasitism of native fishes by co-introduced parasites, which raises questions about the value of remediation actions, such as the removal of introduced hosts, in stemming the rise of infectious disease in species of conservation concern.

Keywords

Biological invasionsdilution effectHawai`ipoeciliidAwaous stamineusCamallanus cotti
Type
Research Article
Information
Parasitology , Volume 143 , Issue 12 , October 2016 , pp. 1605 - 1614
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Blum, M. J., Gilliam, J. F. and McIntyre, P. B. (2014). Development and Use of Genetic Methods for Assessing Aquatic Environmental Condition and Recruitment Dynamics of Native Stream Fishes on Pacific Islands. Final report for the United States Department of Defense, SERDP RC-1646.Google Scholar
Brasher, A. M. (2003). Impacts of human disturbances on biotic communities in Hawaiian streams. BioScience 53, 1052–1060.CrossRefGoogle Scholar
Briggs, C. J., Knapp, R. A. and Vredenburg, V. T. (2010). Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America 107, 9695–9700.CrossRefGoogle ScholarPubMed
Britton, J. R. (2013). Introduced parasites in food webs: new species, shifting structures? Trends in Ecology & Evolution 28, 93–99.CrossRefGoogle ScholarPubMed
Brunner, E. and Munzel, U. (2000). The nonparametric Behrens-fisher problem: asymptotic theory and a small-sample approximation. Biometrical Journal 42, 17–25.3.0.CO;2-U>CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287, 443–449.Google Scholar
Dunn, A. M. and Dick, J. T. (1998). Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography 21, 593–598.Google Scholar
Font, W. F. (2003). The global spread of parasites: what do Hawaiian streams tell us? BioScience 53, 1061–1067.Google Scholar
Font, W. F. (2007). Parasites of Hawaiian stream fishes: sources and impacts. Bishop Museum Bulletin in Cultural and Environmental Studies 3, 157–169.Google Scholar
Font, W. F. and Tate, D. C. (1994). Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolation. Journal of Parasitology 80, 682–688.CrossRefGoogle ScholarPubMed
Frankel, V. M., Hendry, A. P., Rolshausen, G. and Torchin, M. E. (2015). Host preference of an introduced ‘generalist' parasite for a non-native host. International Journal of Parasitology 45, 703–709.Google Scholar
Gagne, R. (2015). Spread of non-native parasites across streams in the Hawaiian archipelago. Doctoral dissertation. Tulane University, School of Science and Engineering, New Orleans, LA, USA.Google Scholar
Gagne, R. B. and Blum, M. J. (2015). Parasitism of a native Hawaiian stream fish by an introduced nematode increases with declining precipitation across a natural rainfall gradient. Ecology of Freshwater Fish 35, 476–486.Google Scholar
Gagne, R. B., Hogan, J. D., Pracheil, B. M., McIntyre, P. B., Hain, E. F., Gilliam, J. F. and Blum, M. J. (2015). Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host. Freshwater Biology 60, 311–322.CrossRefGoogle Scholar
Gastwirth, J., Gel, Y., Hui, W., Lyubchich, V., Miao, W. and Noguchi, K. (2013). lawstat: an R package for biostatistics, public policy, and law. R package version 2.Google Scholar
Giambelluca, T. W., Chen, Q., Frazier, A. G., Price, J. P., Chen, Y.-L., Chu, P.-S., Eischeid, J. K. and Delparte, D. M. (2013). Online rainfall atlas of Hawai'i. Bulletin of the American Meteorological Society 94, 313–316.Google Scholar
Glenn, R. P. and Pugh, T. L. (2006). Epizootic shell disease in American Lobster (Homarus americanus) in Massachusetts Coastal Waters: interactions of temperature, maturity, and Intermolt duration. Journal of Crustacean Biology 26, 639–645.Google Scholar
Gozlan, R. E., St-Hilaire, S., Feist, S. W., Martin, P. and Kent, M. L. (2005). Biodiversity: disease threat to European fish. Nature 435, 1046–1046.CrossRefGoogle ScholarPubMed
Haddaway, N. R., Wilcox, R. H., Heptonstall, R. E., Griffiths, H. M., Mortimer, R. J., Christmas, M. and Dunn, A. M. (2012). Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS ONE 7, e32229.CrossRefGoogle ScholarPubMed
Heins, D. C., Baker, J. A. and Green, D. M. (2011). Processes influencing the duration and decline of epizootics in Schistocephalus solidus . Journal of Parasitology 97, 371–376.CrossRefGoogle ScholarPubMed
Hoffman, G. K. (1999). Parasites of North American Freshwater Fishes. Comstock Publishing Associates, Ithaca, NY.CrossRefGoogle Scholar
Hogan, J. D., McIntyre, P. B., Blum, M. J., Gilliam, J. F. and Bickford, N. (2014). Consequences of alternative dispersal strategies in a putatively amphidromous fish. Ecology 95, 2397–2408.CrossRefGoogle Scholar
Holitzki, T. M., MacKenzie, R. A., Wiegner, T. N. and McDermid, K. J. (2013). Differences in ecological structure, function, and native species abundance between native and invaded Hawaiian streams. Ecological Applications 23, 1367–1383.Google Scholar
Homer, C., Dewitz, J., Fry, J., Coan, M., Hossain, N., Larson, C., Herold, N., McKerrow, A., VanDriel, J. N. and Wickham, J. (2007). Completion of the 2001 national land cover database for the counterminous United States. Photogrammetric Engineering and Remote Sensing 73, 337.Google Scholar
Hutchings, M. R., Athanasiadou, S., Kyriazakis, I. and Gordon, I. J. (2003). Can animals use foraging behaviour to combat parasites?. Proceedings of the Nutrition Society 62, 361–370.Google Scholar
Johnson, P. T. and Thieltges, D. W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961–970.Google Scholar
Johnson, P. T., Carpenter, S. R., Ostfeld, R., Keesing, F. and Eviner, V. (2008). Influence of eutrophication on disease in aquatic ecosystems: patterns, processes, and predictions. Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems 1, 71–79.Google Scholar
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.Google Scholar
Kennedy, C. R., Shears, P. C. and Shears, J. A. (2001). Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123, 257–269.Google Scholar
Kirk, R. (2003). The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology 10, 385–394.CrossRefGoogle Scholar
Lachish, S., Knowles, S. C., Alves, R., Wood, M. J. and Sheldon, B. C. (2011). Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates. Journal of Animal Ecology 80, 1207–1216.Google Scholar
Levsen, A. and Jakobsen, P. J. (2002). Selection pressure towards monoxeny in Camallanus cotti (Nematoda: Camallanidae) facing an intermediate host bottleneck situation. Parasitology 124, 625–629.Google Scholar
Lindstrom, D. P., Blum, M. J., Walter, R. P., Gagne, R. B. and Gilliam, J. F. (2012). Molecular and morphological evidence of distinct evolutionary lineages of Awaous guamensis in Hawai'i and Guam. Copeia 2012, 293–300.Google Scholar
Lo, C. M., Morand, S. and Galzin, R. (1998). Parasite diversity host age and size relationship in three coral-reef fishes from French Polynesia. International Journal of Parasitology 28, 1695–1708.Google Scholar
Menezes, R. C., Tortelly, R., Tortelly-Neto, R., Noronha, D. and Pinto, R. M. (2006). Camallanus cotti Fujita, 1927 (Nematoda, Camallanoidea) in ornamental aquarium fishes: pathology and morphology. Memórias do Instituto Oswaldo Cruz 101, 683–687.Google Scholar
Neuhäuser, M. and Poulin, R. (2004). Comparing parasite numbers between samples of hosts. Journal of Parasitology 90, 689–691.Google Scholar
Parham, J. E., Higashi, G. R., Lapp, E. K., Kuamo'o, D., Nishimoto, R. T., Hau, S., Fitzsimons, J. M., Polhemus, D. A. and Devick, W. S. (2008). Atlas of Hawaiian Watersheds & their aquatic resources. Bishop Museum & Division of Aquatic Resources, Island of Maui 866.Google Scholar
Peeler, E. J. and Feist, S. W. (2011). Human intervention in freshwater ecosystems drives disease emergence. Freshwater Biology 56, 705–716.Google Scholar
Peeler, E. J., Oidtmann, B. C., Midtlyng, P. J., Miossec, L. and Gozlan, R. E. (2010). Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions 13, 1291–1303.Google Scholar
Plowright, R. K., Sokolow, S. H., Gorman, M. E., Daszak, P. and Foley, J. E. (2008). Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6, 420–429.Google Scholar
Prenter, J., Macneil, C., Dick, J. T. and Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385–390.Google Scholar
Price, P. W. and Clancy, K. M. (1983). Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology 69, 449–454.Google Scholar
R Core Team (2012). R: a language and environment for statistical. Computing 14, 12–21.Google Scholar
Reznick, D., Bryant, M. and Holmes, D. (2005). The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol 4, e7.Google Scholar
Sachman-Ruiz, B., Narváez-Padilla, V. and Reynaud, E. (2015). Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México. Biological Invasions 17, 1–11.Google Scholar
Schall, J. J. and Marghoob, A. B. (1995). Prevalence of a malarial parasite over time and space: Plasmodium mexicanum in its vertebrate host, the western fence lizard Sceloporus occidentalis . Journal of Animal Ecology 64, 177–185.Google Scholar
Scharsack, J. P., Kalbe, M., Harrod, C. and Rauch, G. (2007). Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proceedings of the Royal Society B 274, 1523–1532.Google Scholar
Sheath, D. J., Williams, C. F., Reading, A. J. and Britton, J. R. (2015). Parasites of non-native freshwater fishes introduced into England and Wales suggest enemy release and parasite acquisition. Biological Invasions 17, 2235–2246.Google Scholar
Skaug, H., Fournier, D., Nielsen, A. and Magnusson, A. (2006). Package glmmADMB: Generalized linear mixed models using AD Model Builder; software available at http://r-forge.r-project.org/projects/glmmadmb/ Google Scholar
Smith, K., Acevedo-Whitehouse, K. and Pedersen, A. (2009). The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.Google Scholar
Vincent, A. G. and Font, W. F. (2003 a). Host specificity and population structure of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu Stream, O'ahu, Hawai'i. Journal of Parasitology 89, 540–544.Google Scholar
Vincent, A. G. and Font, W. F. (2003 b). Seasonal and yearly population dynamics of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu stream, O'ahu, Hawaii. Journal of Parasitology 89, 756–760.Google Scholar
Violante-González, J., Aguirre-Macedo, M. L. and Vidal-Martínez, V. M. (2008). Temporal variation in the helminth parasite communities of the Pacific fat sleeper, Dormitator latifrons, from Tres Palos Lagoon, Guerrero, Mexico. Journal of Parasitology 94, 326–334.Google Scholar
Walter, R., Hogan, J., Blum, M., Gagne, R., Hain, E., Gilliam, J. and McIntyre, P. (2012). Climate change and conservation of endemic amphidromous fishes in Hawaiian streams. Endangered Species Research 16, 261–272.Google Scholar
Wu, S., Wang, G., Gao, D., Xi, B., Yao, W. and Liu, M. (2007). Occurrence of Camallanus cotti in greatly diverse fish species from Danjiangkou Reservoir in central China. Parasitology Research 101, 467–471.Google Scholar
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