Show simple item record

Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles

dc.contributor.authorSearle, Catherine L.en_US
dc.contributor.authorMendelson, Joseph R.en_US
dc.contributor.authorGreen, Linda E.en_US
dc.contributor.authorDuffy, Meghan A.en_US
dc.date.accessioned2013-11-01T19:01:03Z
dc.date.available2014-11-03T16:20:38Zen_US
dc.date.issued2013-10en_US
dc.identifier.citationSearle, Catherine L.; Mendelson, Joseph R.; Green, Linda E.; Duffy, Meghan A. (2013). " Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles." Ecology and Evolution 3(12): 4129-4138. <http://hdl.handle.net/2027.42/100311>en_US
dc.identifier.issn2045-7758en_US
dc.identifier.issn2045-7758en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/100311
dc.description.abstractDirect predation upon parasites has the potential to reduce infection in host populations. For example, the fungal parasite of amphibians, B atrachochytrium dendrobatidis ( B d), is commonly transmitted through a free‐swimming zoospore stage that may be vulnerable to predation. Potential predators of B d include freshwater zooplankton that graze on organisms in the water column. We tested the ability of two species of freshwater crustacean ( D aphnia magna and D . dentifera ) to consume B d and to reduce B d density in water and infection in tadpoles. In a series of laboratory experiments, we allowed D aphnia to graze in water containing B d while manipulating D aphnia densities, D aphnia species identity, grazing periods and concentrations of suspended algae ( A nkistrodesmus falcatus ). We then exposed tadpoles to the grazed water. We found that high densities of D . magna reduced the amount of Bd detected in water, leading to a reduction in the proportion of tadpoles that became infected. Daphnia dentifera , a smaller species of D aphnia , also reduced B d in water samples, but did not have an effect on tadpole infection. We also found that algae affected B d in complex ways. When D aphnia were absent, less B d was detected in water and tadpole samples when concentrations of algae were higher, indicating a direct negative effect of algae on B d. When D aphnia were present, however, the amount of B d detected in water samples showed the opposite trend, with less B d when densities of algae were lower. Our results indicate that D aphnia can reduce B d levels in water and infection in tadpoles, but these effects vary with species, algal concentration, and D aphnia density. Therefore, the ability of predators to consume parasites and reduce infection is likely to vary depending on ecological context. We tested the ability of two species of freshwater crustacean ( Daphnia magna and D. dentifera ) to consume zoospores of the amphibian parasite, Batrachochytrium dendrobatidis (Bd), and to reduce parasite density in water and infection in tadpoles. In a series of laboratory experiments, we allowed Daphnia to graze in water containing Bd, then exposed tadpoles to the grazed water. Our results show that Daphnia can reduce Bd levels in water and infection in tadpoles, but these effects vary with species, algal concentration and Daphnia density.en_US
dc.publisherR Foundation for Statistical Computingen_US
dc.publisherWiley Periodicals, Inc.en_US
dc.subject.otherParasitesen_US
dc.subject.otherL Ithobates Sphenocephalusen_US
dc.subject.otherTrophic Interactionsen_US
dc.subject.otherB Atrachochytrium Dendrobatidisen_US
dc.subject.otherChytridiomycosisen_US
dc.subject.otherEutrophicationen_US
dc.titleDaphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpolesen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelEcology and Evolutionary Biologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/100311/1/ece3777.pdf
dc.identifier.doi10.1002/ece3.777en_US
dc.identifier.sourceEcology and Evolutionen_US
dc.identifier.citedreferenceNelson, X. J. and R. R. Jackson. 2006. A predator from East Africa that chooses malaria vectors as preferred prey. PLoS ONE 1: e132.en_US
dc.identifier.citedreferenceKluttgen, B., U. Dulmer, M. Engels, and H. T. Ratte. 1994. ADaM, an artificial freshwater for the culture of zooplankton. Water Res. 28: 743 – 746.en_US
dc.identifier.citedreferenceKwik, J. K., and J. C. H. Carter. 1975. Population dynamics of limnetic Cladocera in a beaver pond. J. Fish. Res. Board Can. 32: 341 – 346.en_US
dc.identifier.citedreferenceLafferty, K. D. 2004. Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol. Appl. 14: 1566 – 1573.en_US
dc.identifier.citedreferenceLafferty, K. D., A. P. Dobson, and A. M. Kuris. 2006. Parasites dominate food web links. Proc. Natl Acad. Sci. USA 103: 11211 – 11216.en_US
dc.identifier.citedreferenceLam, B. A., J. B. Walke, V. T. Vredenburg, and R. N. Harris. 2010. Proportion of individuals with anti‐ Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol. Conserv. 143: 529 – 531.en_US
dc.identifier.citedreferenceLips, K. R., F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, et al. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl Acad. Sci. USA 103: 3165 – 3170.en_US
dc.identifier.citedreferenceLongcore, J. E., A. P. Pessier, and D. K. Nichols. 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91: 219 – 227.en_US
dc.identifier.citedreferenceLuecke, C., M. J. Vanni, J. J. Magnuson, J. F. Kitchell, and P. T. Jacobson. 1990. Seasonal regulation of Daphnia populations by planktivorous fish: implications for the spring clear‐water phase. Limnol. Oceanogr. 8: 1718 – 1733.en_US
dc.identifier.citedreferenceOmacini, M., E. J. Chaneton, C. M. Ghersa, and C. B. Muller. 2001. Symbiotic fungal endophytes control insect host‐parasite interaction webs. Nature 409: 78 – 81.en_US
dc.identifier.citedreferenceOrlofske, S. A., R. C. Jadin, D. L. Preston, and P. T. J. Johnson. 2012. Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93: 1247 – 1253.en_US
dc.identifier.citedreferencePacker, C., R. D. Holt, P. J. Hudson, K. D. Lafferty, and A. P. Dobson. 2003. Keeping herds healthy and alert: implications of predator control for infectious disease. Ecol. Lett. 6: 797 – 802.en_US
dc.identifier.citedreferencePiotrowski, J. S., S. L. Annis, and J. E. Longcore. 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96: 9 – 15.en_US
dc.identifier.citedreferencePorter, K. G. 1973. Selective grazing and differential digestion of algae by zooplankton. Nature 244: 179 – 180.en_US
dc.identifier.citedreferencePorter, K. G. 1976. Enhancement of algal growth and productivity by grazing zooplankton. Science 192: 1332 – 1334.en_US
dc.identifier.citedreferenceR Core Development Team. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3‐900051‐07‐0, Available at http://www.R-project.org/.en_US
dc.identifier.citedreferenceRamirez, R. A. and W. E. Snyder. 2009. Scared sick? Predator‐pathogen facilitation enhances exploitation of a shared resource. Ecology 90: 2832 – 2839.en_US
dc.identifier.citedreferenceRowley, J. J. L. and R. A. Alford. 2007. Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Dis. Aquat. Org. 77: 1 – 9.en_US
dc.identifier.citedreferenceSchloegel, L. M., C. M. Ferreira, T. Y. James, M. Hipolito, J. E. Longcore, A. D. Hyatt, et al. 2009. The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Anim. Conserv. 13 s1: 53 – 61.en_US
dc.identifier.citedreferenceSearle, C. L., S. S. Gervasi, J. Jua, J. I. Hammond, R. A. Relyea, D. H. Olson, et al. 2011. Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conserv. Biol. 25: 965 – 974.en_US
dc.identifier.citedreferenceSkerratt, L. F., L. Berger, R. Spear, S. Cashins, K. R. McDonald, A. D. Phillott, et al. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4: 125 – 134.en_US
dc.identifier.citedreferenceWake, D. B. and V. T. Vredenburg. 2008. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl Acad. Sci. USA 105: 11466 – 11473.en_US
dc.identifier.citedreferenceWolfe, J. M. and E. L. Rice. 1979. Allelopathic interactions among algae. J. Chem. Ecol. 5: 533 – 542.en_US
dc.identifier.citedreferenceWoodhams, D. C., J. Bosch, C. J. Briggs, S. Cashins, L. R. Davis, A. Lauer, et al. 2011. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front. Zool. 8: 8.en_US
dc.identifier.citedreferenceZuur, A., E. N. Ieno, N. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extensions in ecology with R, 1st edn. Springer, New York, NY.en_US
dc.identifier.citedreferenceBosch, J., I. Martinez‐Solano, and M. Garcia‐Paris. 2001. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad ( Alytes obstetricans ) in protected areas of central Spain. Biol. Conserv. 97: 331 – 337.en_US
dc.identifier.citedreferenceBottrell, H. H., A. Duncan, Z. M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbright‐Ilkowska, et al. 1976. A review of some problems in zooplankton production studies. Norw. J. Zool. 24: 419 – 456.en_US
dc.identifier.citedreferenceBoyle, D. G., D. B. Boyle, V. Olsen, J. A. T. Morgan, and A. D. Hyatt. 2004. Rapid quantitative detection of chytridiomycosis ( Batrachochytrium dendrobatidis ) in amphibian samples using real‐time Taqman PCR assay. Dis. Aquat. Org. 60: 141 – 148.en_US
dc.identifier.citedreferenceBuck, J. C., L. Truong, and A. R. Blaustein. 2011. Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus? Biodivers. Conserv. 20: 3549 – 3553.en_US
dc.identifier.citedreferenceBurns, C. W. 1968. The relationship between body size of filter‐feeding Cladocera and the maximum size of particle ingested. Limnol. Oceanogr. 13: 675 – 678.en_US
dc.identifier.citedreferenceBurns, C. W. 1969. Relation between filtering rate, temperature, and body size in four species of Daphnia. Limnol. Oceanogr. 14: 693 – 700.en_US
dc.identifier.citedreferenceDawes, C. J., B. C. Cowell, W. E. Gardiner, and S. M. Scheda. 1987. Limnological characteristics of two eutrophic and four mesotrophic lakes in west‐central Florida. Int. Rev. Hydrobiol. 72: 171 – 203.en_US
dc.identifier.citedreferenceDeMott, W. R. 1983. Seasonal succession in a natural Daphnia assemblage. Ecol. Monogr. 53: 321 – 340.en_US
dc.identifier.citedreferenceDeMott, W. R. and R. D. Gulati. 1999. Phosphorus limitation in Daphnia: evidence from a long term study of three hypereutrophic Dutch lakes. Limnol. Oceanogr. 6: 1557 – 1564.en_US
dc.identifier.citedreferenceDeMott, W. R., E. N. McKinney, and A. J. Tessier. 2010. Ontogeny of digestion in Daphnia: implications for the effectiveness of algal defenses. Ecology 91: 540 – 548.en_US
dc.identifier.citedreferenceDuffy, M. A., S. R. Hall, A. J. Tessier, and M. Huebner. 2005. Selective predators and their parasitized prey: are epidemics in zooplankton under top‐down control? Limnol. Oceanogr. 50: 412 – 420.en_US
dc.identifier.citedreferenceDuffy, M. A., J. M. Housley, R. M. Penczykowski, C. E. Caceres, and S. R. Hall. 2011. Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Funct. Ecol. 25: 945 – 953.en_US
dc.identifier.citedreferenceGeller, W., and H. Muller. 1981. The filtration apparatus of Cladocera: filter mesh‐sizes and their implications on food selectivity. Oecologia 49: 316 – 321.en_US
dc.identifier.citedreferenceGervasi, S., C. Gondhalekar, D. H. Olson, and A. R. Blasutein. 2013. Host identity matters in the amphibian‐ Batrachochytrium dendrobatidis system: fine‐scale patterns of variation in responses to a multi‐host pathogen. PLoS ONE 8: e54490.en_US
dc.identifier.citedreferenceGrutter, A. 1996. Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar. Ecol. Prog. Ser. 130: 61 – 70.en_US
dc.identifier.citedreferenceHall, S. R., L. Sivars‐Becker, C. Becker, M. A. Duffy, A. J. Tessier, and C. E. Caceres. 2007. Eating yourself sick: transmission of disease as a function of foraging ecology. Ecol. Lett. 10: 207 – 218.en_US
dc.identifier.citedreferenceHall, S. R., C. R. Becker, M. A. Duffy, and C. E. Caceres. 2010. Variation in resource acquisition and use among host clones creates key epidemiological trade‐offs. Am. Nat. 176: 557 – 565.en_US
dc.identifier.citedreferenceHamilton, P. T., J. M. L. Richardson, and B. R. Anholt. 2012. Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis. Freshw. Biol. 57: 676 – 683.en_US
dc.identifier.citedreferenceHaney, J. F. 1987. Field studies on zooplankton‐cyanobacteria interactions. N. Z. J. Mar. Freshwater Res. 21: 467 – 475.en_US
dc.identifier.citedreferenceHarris, R. N., T. Y. James, A. Lauer, M. A. Simon, and A. Patel. 2006. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. EcoHealth 3: 53 – 56.en_US
dc.identifier.citedreferenceHoward, A. F. V., G. Zhou, and F. X. Omlin. 2007. Malaria mosquito control using edible fish in western Kenya: preliminary findings of a controlled study. BMC Public Health 7: 199.en_US
dc.identifier.citedreferenceJohnson, M. L., and R. Speare. 2003. Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg. Infect. Dis. 9: 922 – 925.en_US
dc.identifier.citedreferenceKagami, M., E. V. Donk, A. de Bruin, M. Rijkeboer, and B. W. Ibelings. 2004. Daphnia can protect diatoms from fungal parasitism. Limnol. Oceanogr. 49: 680 – 685.en_US
dc.identifier.citedreferenceKeesing, F., R. D. Holt, and R. S. Ostfeld. 2006. Effects of species diversity on disease risk. Ecol. Lett. 9: 485 – 498.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.