Skip to main content

Advertisement

Log in

Combined Effects of Virus, Pesticide, and Predator Cue on the Larval Tiger Salamander (Ambystoma tigrinum)

  • Original contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Emerging diseases and environmental contamination are two of the leading hypotheses for global amphibian declines. Yet few studies have examined the influence of contaminants on disease susceptibility, and even fewer have incorporated the role of natural stressors such as predation. We performed a factorial study investigating the interaction of the insecticide carbaryl, dragonfly predator cue, and the emerging pathogen Ambystoma tigrinum virus (ATV) on fitness correlates and disease susceptibility in tiger salamander larvae. Four week old larvae were exposed for 22 days in a 2 (0, 500 μg/l carbaryl) × 2 (control, predator cue water) × 2 (0, 1 × 104 pfu ATV) factorial designed laboratory study. Results show significant impacts to survival of larvae for both virus and predator cue treatments, as well as an interactive effect between the two, in which predator cue strongly exacerbated disease-driven mortality. There was a clear pattern of reduced survival with the addition of stressors, with those where all three stressors were present exhibiting the worst effects (a decrease in survival from 93 to 60%). On those that survived, we also detected several sub-lethal impacts in mass, SVL, and development. Predator cue and pesticide treatments significantly reduced both SVL and mass. Virus and predator treatments significantly slowed development. Stressors also exhibited opposing effects on activity. Predator cue caused a significant reduction in activity, whereas virus caused a significant increase in activity over time. These results highlight the importance of examining combined natural and introduced stressors to understand potential impacts on amphibian species. Such stressors may contribute to the emergence of ATV in particular regions, raising concerns about the influence of pesticides on disease emergence in general.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Belden L, and Kiesecker J (2005). Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. Journal of Parasitology 91:686-688.

    Article  PubMed  CAS  Google Scholar 

  • Belden L, Moore I, Mason R, Wingfield J, and Blaustein A (2003). Survival, the hormonal stress response and UV-B avoidance in Cascades Frog tadpoles (Rana cascadae) exposed to UV-B radiation. Functional Ecology 17:409-416.

    Article  Google Scholar 

  • Bradford DF, Stanley K, McConnell LL, Tallent-Halsell NG, Nash MS, Simonich SM (2010) Spatial patterns of atmospherically deposited organic contaminants at high-elevation in the southern Sierra Nevada mountains, California, USA. Environmental Toxicology and Chemistry 29:1056–1066.

    PubMed  CAS  Google Scholar 

  • Brunner J, Richards K, and Collins J (2005). Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144:399-406.

    Article  PubMed  Google Scholar 

  • Collins J, and Storfer A (2003). Global amphibian declines: sorting the hypotheses. Diversity & Distributions 9:89-98.

    Article  Google Scholar 

  • Das K, Roy S, and Chattopadhyay J (2008). Effect of disease-selective predation on prey infected by contact and external sources. BioSystems 95:188–199

    Article  PubMed  Google Scholar 

  • Daszak P, Cunningham A, and Hyatt A (2000). Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287:443.

    Article  PubMed  CAS  Google Scholar 

  • Daszak P, Cunningham A, and Hyatt A (2003). Infectious disease and amphibian population declines. Diversity and Distributions 9:141-150.

    Article  Google Scholar 

  • de Castro F, and Bolker B (2005). Parasite establishment and host extinction in model communities. Oikos 111:501-513.

    Article  Google Scholar 

  • Fenton A, Fairbairn J, Norman R, and Hudson P (2002). Parasite transmission: reconciling theory and reality. Journal of Animal Ecology 71:893-905.

    Article  Google Scholar 

  • Fisher M, Garner T, and Walker S (2009). Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63:291–310

    Article  PubMed  CAS  Google Scholar 

  • Fleischli M, Franson J, Thomas N, Finley D, and Riley W (2004). Avian mortality events in the United States caused by anticholinesterase pesticides: a retrospective summary of National Wildlife Health Center records from 1980 to 2000. Archives of environmental contamination and toxicology 46:542-550.

    Article  PubMed  CAS  Google Scholar 

  • Forson D, and Storfer A (2006a). Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecological Applications 16:2325-2332.

    Article  PubMed  Google Scholar 

  • Forson D, and Storfer A (2006b). Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed salamander (Ambystoma macrodactylum). Environmental Toxicology and Chemistry 25:168-173.

    Article  PubMed  CAS  Google Scholar 

  • Green D, Converse K, and Schrader A (2002). Epizootiology of Sixty Four Amphibian Morbidity and Mortality Events in the USA, 1996 2001. Annals of the New York Academy of Sciences 969:323-339.

    Article  PubMed  Google Scholar 

  • Grenfell B, Dobson A (1995) Ecology of infectious diseases in natural populations. Cambridge Univ Press, Cambridge

    Book  Google Scholar 

  • Hudson P, and Greenman J (1998). Competition mediated by parasites: biological and theoretical progress. Trends in Ecology & Evolution 13:387.

    Article  CAS  Google Scholar 

  • Jancovich J, Davidson E, Parameswaran N, Mao J, Chinchar V, Collins J, et al. (2005). Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Molecular Ecology 14:213-224.

    Article  PubMed  CAS  Google Scholar 

  • Kats L, and Dill L (1998). The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361-394.

    Google Scholar 

  • Kerby J, and Storfer A (2009). Combined Effects of Atrazine and Chlorpyrifos on Susceptibility of the Tiger Salamander to Ambystoma tigrinum Virus. EcoHealth 6:91–98

    Article  PubMed  Google Scholar 

  • Knutson M, Richardson W, Reineke D, Gray B, Parmelee J, and Weick S (2004). Agricultural ponds support amphibian populations. Ecological Applications 14:669-684.

    Article  Google Scholar 

  • Lafferty K, Dobson A, and Kuris A (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences 103:11211.

    Article  CAS  Google Scholar 

  • Lips K, Diffendorfer J, Mendelson III J, and Sears M (2008). Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol 6:e72.

    Article  PubMed  Google Scholar 

  • McCallum H, and Dobson A (1995). Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology & Evolution 10:190-194.

    Article  CAS  Google Scholar 

  • Norris L, Lorz H, Gregory S (1983) Influence of forest and range land management on anadromous fish habitat in western North America: forest chemicals. General technical report PNW, Portland, OR

  • Parris M, Beaudoin J (2004) Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140:626–632

    Article  PubMed  Google Scholar 

  • Parris M, Davis A, and Collins J (2004). Single-host pathogen effects on mortality and behavioral responses to predators in salamanders (Urodela: Ambystomatidae). Canadian Journal of Zoology 82:1477-1483.

    Article  Google Scholar 

  • Peterson H, Boutin C, Martin P, Freemark K, Ruecker N, and Moody M (1994). Aquatic phyto-toxicity of 23 pesticides applied at expected environmental concentrations. Aquatic Toxicology 28:275-292.

    Article  CAS  Google Scholar 

  • Pfennig D, Ho S, and Hoffman E (1998). Pathogen transmission as a selective force against cannibalism. Animal Behaviour 55:1255-1261.

    Article  PubMed  Google Scholar 

  • Picco A, and Collins J (2008). Amphibian Commerce as a Likely Source of Pathogen Pollution. Conservation Biology 22:1582.

    Article  PubMed  Google Scholar 

  • Pounds J, Bustamante M, Coloma L, Consuegra J, Fogden M, Foster P, et al. (2006). Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161-167.

    Article  PubMed  CAS  Google Scholar 

  • Raffel T, Hoverman J, Halstead N, Michel P, Rohr J (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 91:1900–1907

    Article  PubMed  Google Scholar 

  • Relyea R (2003). Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13:1515-1521.

    Article  Google Scholar 

  • Relyea R (2009). A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363-376.

    Article  PubMed  Google Scholar 

  • Relyea R, and Mills N (2001). Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences 98:2491.

    Article  CAS  Google Scholar 

  • Ridenhour B, and Storfer A (2008). Geographically variable selection in Ambystoma tigrinum virus (Iridoviridae) throughout the western USA. Journal of evolutionary biology 21:1151-1159.

    Article  PubMed  CAS  Google Scholar 

  • Rohr J, Raffel T, Romansic J, McCallum H, and Hudson P (2008). Evaluating the links between climate, disease spread, and amphibian declines. Proceedings of the National Academy of Sciences 105:17436.

    Article  CAS  Google Scholar 

  • Sih A, Bell A, and Kerby J (2004a). Two stressors are far deadlier than one. Trends in Ecology & Evolution 19:274-276.

    Article  Google Scholar 

  • Sih A, Kerby J, Bell A, and Relyea R (2004b). Response to Schmidt. Pesticides, mortality and population growth rate. Trends in Ecology & Evolution 19:460-461.

    Article  Google Scholar 

  • Storfer A, Alfaro M, Ridenhour B, Jancovich J, Mech S, Parris M, et al. (2007). Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic. Ecology Letters 10:1075-1083.

    Article  PubMed  Google Scholar 

  • Stuart S, Chanson J, Cox N, Young B, Rodrigues A, Fischman D, et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786.

    Article  PubMed  CAS  Google Scholar 

  • Watson S, Russell A (2000) A posthatching developmental staging table for the long-toed salamander, Ambystoma macrodactylum krausei. Amphibia-Reptilia 21:143–154

    Article  Google Scholar 

  • Werner E, and Anholt B (1993). Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. American Naturalist 142:242.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Thanks to the Center for Integrated Biotechnology and NSF grant 0548415 to A.S. for their sponsorship of this research. We would also like to thank K. Benyo, J. Cotter, and J. Eastman for collecting tiger salamander larvae; and J. Baumsteiger, R. Featherkile, R. Artest, A. McCally, and N. Sinacore for their logistic help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jacob L. Kerby.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kerby, J.L., Hart, A.J. & Storfer, A. Combined Effects of Virus, Pesticide, and Predator Cue on the Larval Tiger Salamander (Ambystoma tigrinum). EcoHealth 8, 46–54 (2011). https://doi.org/10.1007/s10393-011-0682-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-011-0682-1

Keywords

Navigation