Skip to main content

Effects of Lead Exposure, Flock Behavior, and Management Actions on the Survival of California Condors (Gymnogyps californianus)

Abstract

Translocation is an increasingly important tool for managing endangered species, but factors influencing the survival of translocated individuals are not well understood. Here we examine intrinsic and extrinsic drivers of survival for critically endangered California condors (Gymnogyps californianus) whose wild population recovery is reliant upon releases of captively bred stock. We used known fate models and information-theoretic methods to compare the ability of hypothesized covariates, most of which serve as proxies for lead exposure risk, to predict survival rates of condors in California. Our best supported model included the following predictors of survival: age of the recovery program, precipitation, proportion of days observed feeding on proffered carcasses, maximum blood lead concentration over the preceding 18 months, and time since release. We found that as flocks have increased in size and age, condors are increasingly likely to range more widely and less likely to be observed feeding on proffered food, and these “wilder” behaviors were associated with lower survival. After accounting for these behaviors, we found a positive survival trend, which we attribute to ongoing improvements in management. Our findings illustrate that the survival of translocated animals, such as highly social California condors, is influenced by behaviors that change through time.

This is a preview of subscription content, access via your institution.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

References

  1. Bakker VJ, Doak DF, Roemer GW, Garcelon DK, Coonan TJ, Morrison SA, et al. (2009). Incorporating ecological drivers and uncertainty into a demographic population viability analysis for the island fox. Ecological Monographs 79:77-108.

    Article  Google Scholar 

  2. Brown CR (1986). Cliff swallow colonies as information-centers. Science 234:83-85.

    CAS  Article  PubMed  Google Scholar 

  3. Buckley NJ (1997). Experimental tests of the information-center hypothesis with black vultures (Coragyps atratus) and turkey vultures (Cathartes aura). Behavioral Ecology and Sociobiology 41:267-279.

    Article  Google Scholar 

  4. Burnett LJ, Sorenson KJ, Brandt J, Sandhaus EA, Ciani D, Clark M, et al. (2013). Eggshell thinning and depressed hatching success of California condors reintroduced to central California. Condor 115:477-491.

    Article  Google Scholar 

  5. Burnham KP, and Anderson D (2002). Model Selection and Multi-Model Inference, 2nd edition. Spring-Verlag, New York.

    Google Scholar 

  6. Burnham KP, Anderson DR, and Huyvaert KP (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65:23-35.

    Article  Google Scholar 

  7. Cade TJ (2007). Exposure of California condors to lead from spent ammunition. Journal of Wildlife Management 71:2125-2133.

    Article  Google Scholar 

  8. Cooch E, and White G (editors) (2010) Program MARKAnalysis of Data from Marked IndividualsA Gentle Introduction, 9th edition. http://www.cnr.colostate.edu/~gwhite/mark/mark.htm.

  9. Coonan TJ, Schwemm CA, and Garcelon DK (2010). Decline and recovery of the island fox: a case study for population recovery. New York: Cambridge University Press.

    Book  Google Scholar 

  10. Fieberg J, and DelGiudice GD (2009). What time is it? Choice of time origin and scale in extended proportional hazards models. Ecology 90:1687-1697.

    Article  PubMed  Google Scholar 

  11. Finkelstein ME, Brandt J, Sandhaus EA, Grantham J, Mee A, Schuppert PJ, et al. (2015). Lead exposure risk from trash ingestion by the endangered California condor (Gymnogyps californianus) Journal of Wildlife Diseases 51: 901-906.

    CAS  Article  PubMed  Google Scholar 

  12. Finkelstein ME, Doak DF, George D, Burnett J, Brandt J, Church M, et al. (2012). Lead poisoning and the deceptive recovery of the critically endangered California condor. Proceedings of the National Academy of Sciences 29: 11449-11454.

    Article  Google Scholar 

  13. Finkelstein ME, George D, Scherbinski S, Gwiazda R, Johnson M, Burnett J, et al. (2010) Feather lead concentrations and (207)Pb/(206)Pb ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environmental Science & Technology 44:2639–2647

    CAS  Article  Google Scholar 

  14. Grantham J (2007) Reintroduction of California Condors into their historic range: the recovery program in California. In: California Condors in the 21st Century, Mee A and Hall LS (editors). American Ornithologists Union, pp 123–138.

  15. Green RE, Hunt WG, Parish CN, and Newton I (2008). Effectiveness of Action to Reduce Exposure of Free-Ranging California Condors in Arizona and Utah to Lead from Spent Ammunition. PLOS One 3: e4022.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Grenier MB, McDonald DB, and Buskirk SW (2007). Rapid population growth of a critically endangered carnivore. Science 317:779.

    CAS  Article  PubMed  Google Scholar 

  17. Halekoh U, Hojsgaard S, and Yan J (2006). The R Package geepack for Generalized Estimating Equations. Journal of Statistical Software 15:1-11.

    Article  Google Scholar 

  18. Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, et al. (2008). Assisted colonization and rapid climate change. Science 321:345-346.

    CAS  Article  PubMed  Google Scholar 

  19. Kelly TR, Grantham J, George D, Welch A, Brandt J, Burnett LJ, et al. (2014). Spatiotemporal patterns and risk factors for lead exposure in endangered California condors during 15 Years of reintroduction. Conservation Biology 28:1721-1730.

    Article  PubMed  Google Scholar 

  20. Kelly TR, Rideout BA, Grantham J, Brandt J, Burnett LJ, Sorenson KJ, et al. (2015). Two decades of cumulative impacts to survivorship of endangered California condors in California. Biological Conservation 191:391-399.

    Article  Google Scholar 

  21. Lebreton JD, Burnham KP, Clobert J, and Anderson DR (1992). Modeling survival and testing biological hypotheses using marked animals a unified approach with case studies. Ecological Monographs 62:67-118.

    Article  Google Scholar 

  22. Marshal JP, and Bleich VC (2011). Evidence of relationships between El Nino Southern Oscillation and mule deer harvest in California. California Fish and Game 97:84-97.

    Google Scholar 

  23. Marshal JP, Krausman RP, Bleich VC, Ballard WB, and McKeever JS (2002). Rainfall, El Nino, and dynamics of mule deer in the Sonoran Desert, California. Journal of Wildlife Management 66:1283-1289.

    Article  Google Scholar 

  24. Marzluff JM, Heinrich B, and Marzluff CS (1996). Raven roosts are mobile information centres. Animal Behaviour 51:89-103.

    Article  Google Scholar 

  25. Meretsky VJ, Snyder NFR, Beissinger SR, Clendenen DA, and Wiley JW (2000). Demography of the California Condor: Implications for reestablishment. Conservation Biology 14:957-967.

    Article  Google Scholar 

  26. Pan W (2001). Akaike’s information criterion in generalized estimating equations. Biometrics 57:120-125.

    CAS  Article  PubMed  Google Scholar 

  27. Pinter-Wollman N, Isbell LA, and Hart LA (2009). The relationship between social behaviour and habitat familiarity in African elephants (Loxodonta africana). Proceedings of the Royal Society B-Biological Sciences 276:1009-1014.

    Article  Google Scholar 

  28. PRISM Group (2015). Time series dataset. PRISM Climate Group, Oregon State University. http://prism.oregonstate.edu, generated 9 Oct 2015.

  29. Rideout BA, Stalis I, Papendick R, Pessier A, Puschner B, Finkelstein ME, et al. (2012). Patterns of mortality in free-ranging California condors (Gymnogyps californianus). Journal of Wildlife Diseases 48:95-112.

    Article  PubMed  Google Scholar 

  30. Ridley-Tree Condor Preservation Act (2008). In Assembly Bill No. 821. Pages 95 in Chapter 570.

  31. Rivers JW, Johnson JM, Haig SM, Schwarz CJ, Burnett LJ, Brandt J, et al. (2014). An analysis of monthly home range size in the critically endangered California Condor Gymnogyps californianus. Bird Conservation International 24:492-504.

    Article  Google Scholar 

  32. Rivrud IM, Meisingset EL, Loe LE, and Mysterud A (2014). Interaction effects between weather and space use on harvesting effort and patterns in red deer. Ecology and Evolution 4:4786-4797.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Sheppard JK, Walenski M, Wallace MP, Velazco JJV, Porras C, and Swaisgood RR (2013). Hierarchical dominance structure in reintroduced California condors: correlates, consequences, and dynamics. Behavioral Ecology and Sociobiology 67:1227-1238.

    Article  Google Scholar 

  34. Shier DM (2006). Effect of family support on the success of translocated black-tailed prairie dogs. Conservation Biology 20:1780-1790.

    CAS  Article  PubMed  Google Scholar 

  35. Skerfving S, and Bergdahl IA (2014). Lead. In: Handbook on the Toxicology of Metals, Nordberg M, Nordberg GF, Fowler BA, and Friberg L (editors), 4th edn, pp 911–967.

  36. U.S. Fish and Wildlife Service [USFWS] (2012) Hopper Mountain National Wildlife Refuge Complex California Condor Recovery Program annual report. http://www.fws.gov/uploadedFiles/Region_8/NWRS/Zone_1/Hopper_Mountain_Complex/Hopper_Mountain/Sections/What_We_Do/Conservation/PDFs/USFWS_CondorProg_%20AnnReport%202012.pdf. Accessed June 2015, Ventura, CA.

  37. U.S. Fish and Wildlife Service [USFWS] (2013). California Condor (Gymnogyps californianus) 5-year review: summary and evaluation, Ventura, CA.

    Google Scholar 

  38. Utt AC, Harvey NC, Hayes WK, and Carter RL (2008). The effects of rearing method on social behaviors of mentored, captive-reared juvenile California condors. Zoo Biology 27:1-18.

    Article  PubMed  Google Scholar 

  39. Walters JR, Derrickson SR, Fry DM, Haig SM, Marzluff JM, and Wunderle JM, Jr. (2010). Status of the California condor (Gymnogyps californianus) and efforts to achieve its recovery. Auk 127:969-1001.

    Article  Google Scholar 

  40. Wright J, Stone RE, and Brown N (2003). Communal roosts as structured information centres in the raven, Corvus corax. Journal of Animal Ecology 72:1003-1014.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the United States Fish and Wildlife Service California Condor Recovery Program, The Nature Conservancy, The Zoological Society of London, and field crews associated with Pinnacles National Park, Ventana Wildlife Society, and the Hopper Mountain National Wildlife Refuge Complex. Special thanks to T. Kelly, D. Moen, B. Rideout, S. Scherbinski, and A. Welch for their important contributions to this study. We are also grateful to D. Doak and three anonymous reviewers for providing helpful comments on an earlier manuscript draft. This project was supported by the U.S. Fish and Wildlife Service. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Myra E. Finkelstein.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 99 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bakker, V.J., Smith, D.R., Copeland, H. et al. Effects of Lead Exposure, Flock Behavior, and Management Actions on the Survival of California Condors (Gymnogyps californianus). EcoHealth 14, 92–105 (2017). https://doi.org/10.1007/s10393-015-1096-2

Download citation

Keywords

  • lead exposure
  • survival
  • California condor
  • management actions
  • flock
  • precipitation
  • translocation