Skip to main content Accessibility help
×
Home
Hostname: page-component-78bd46657c-2z7pd Total loading time: 0.193 Render date: 2021-05-10T08:58:02.656Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Article contents

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
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
E-mail address:

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.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below.

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, 10521060.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, 96959700.CrossRefGoogle ScholarPubMed
Britton, J. R. (2013). Introduced parasites in food webs: new species, shifting structures? Trends in Ecology & Evolution 28, 9399.CrossRefGoogle ScholarPubMed
Brunner, E. and Munzel, U. (2000). The nonparametric Behrens-fisher problem: asymptotic theory and a small-sample approximation. Biometrical Journal 42, 1725.3.0.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, 575583.CrossRefGoogle Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287, 443449.CrossRefGoogle ScholarPubMed
Dunn, A. M. and Dick, J. T. (1998). Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography 21, 593598.CrossRefGoogle Scholar
Font, W. F. (2003). The global spread of parasites: what do Hawaiian streams tell us? BioScience 53, 10611067.CrossRefGoogle Scholar
Font, W. F. (2007). Parasites of Hawaiian stream fishes: sources and impacts. Bishop Museum Bulletin in Cultural and Environmental Studies 3, 157169.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, 682688.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, 703709.CrossRefGoogle ScholarPubMed
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, 476486.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, 311322.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, 313316.CrossRefGoogle 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, 639645.CrossRefGoogle 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, 10461046.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, 371376.CrossRefGoogle ScholarPubMed
Hoffman, G. K. (1999). Parasites of North American Freshwater Fishes. Comstock Publishing Associates, Ithaca, NY.Google 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, 23972408.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, 13671383.CrossRefGoogle ScholarPubMed
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, 361370.CrossRefGoogle ScholarPubMed
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, 961970.CrossRefGoogle ScholarPubMed
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, 7179.Google Scholar
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485498.CrossRefGoogle ScholarPubMed
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, 257269.CrossRefGoogle ScholarPubMed
Kirk, R. (2003). The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology 10, 385394.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, 12071216.CrossRefGoogle 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, 625629.CrossRefGoogle 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, 293300.CrossRefGoogle 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, 16951708.CrossRefGoogle ScholarPubMed
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, 683687.CrossRefGoogle ScholarPubMed
Neuhäuser, M. and Poulin, R. (2004). Comparing parasite numbers between samples of hosts. Journal of Parasitology 90, 689691.CrossRefGoogle ScholarPubMed
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, 705716.CrossRefGoogle 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, 12911303.CrossRefGoogle 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, 420429.CrossRefGoogle 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, 385390.CrossRefGoogle ScholarPubMed
Price, P. W. and Clancy, K. M. (1983). Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology 69, 449454.CrossRefGoogle Scholar
R Core Team (2012). R: a language and environment for statistical. Computing 14, 1221.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.CrossRefGoogle 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, 111.CrossRefGoogle 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, 177185.CrossRefGoogle 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, 15231532.CrossRefGoogle ScholarPubMed
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, 22352246.CrossRefGoogle 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, 112.CrossRefGoogle 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, 540544.CrossRefGoogle 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, 756760.CrossRefGoogle 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, 326334.CrossRefGoogle ScholarPubMed
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, 261272.CrossRefGoogle 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, 467471.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gagne supplementary material

Figures S1-S3

Download Gagne supplementary material(File)
File 319 KB

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

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

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

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

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *