Abstract
Increasing urbanization and use of urban areas by synanthropic wildlife has increased human and domestic animal exposure to zoonotic diseases and exacerbated epizootics within wildlife populations. Consequently, there is a need to improve wildlife disease surveillance programs to rapidly detect outbreaks and refine inferences regarding spatiotemporal disease dynamics. Multistate occupancy models can address potential shortcomings in surveillance programs by accounting for imperfect detection and the misclassification of disease states. We used these models to explore the relationship between urbanization, slope, and the spatial distribution of sarcoptic mange in coyotes (Canis latrans) inhabiting Fort Irwin, California, USA. We deployed remote cameras across 180 sites within the desert surrounding the populated garrison and classified sites by mange presence or absence depending on whether a symptomatic or asymptomatic coyote was photographed. Coyotes selected flatter sites closer to the urban area with a high probability of use (0.845, 95% credible interval (CRI): 0.728, 0.944); site use decreased as the distance to urban areas increased (standardized \({\widehat{\beta}}\) = − 1.354, 95% CRI − 2.423, − 0.619). The probability of correctly classifying mange presence at a site also decreased further from the urban area and was probably related to the severity of mange infection. Severely infected coyotes, which were more readily identified as symptomatic, resided closer to the urban area and were most likely dependent on urban resources for survival; urban resources probably contributed to sustaining the disease. Multistate occupancy models represent a flexible framework for estimating the occurrence and spatial extent of observable infectious diseases, which can improve wildlife disease surveillance programs.
Similar content being viewed by others
References
Adams MJ, Chelgren ND, Reinitz D et al (2010) Using occupancy models to understand the distribution of an amphibian pathogen, Batrachochytrium dendrobatidis. Ecol Appl 20:289–302. https://doi.org/10.1890/08-2319.1
Allen T, Murray KA, Zambrana-Torrelio C et al (2017) Global hotspots and correlates of emerging zoonotic diseases. Nat Commun 8:1124. https://doi.org/10.1038/s41467-017-00923-8
Almberg ES, Cross PC, Dobson AP et al (2012) Parasite invasion following host reintroduction: a case study of Yellowstone’s wolves. Philos Trans R Soc Lond B Biol Sci 367:2840–2851. https://doi.org/10.1098/rstb.2011.0369
Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287:1–23. https://doi.org/10.1111/j.1469-7998.2011.00887.x
Becker DJ, Streicker DG, Altizer S (2015) Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecol Lett 18:483–495. https://doi.org/10.1111/ele.12428
Blehert DS, Hicks AC, Behr M et al (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227. https://doi.org/10.1126/science.1163874
Bleich VC (1999) Mountain sheep and coyotes: patterns of predator evasion in a mountain ungulate. J Mammal 80:283–289. https://doi.org/10.2307/1383228
Bornstein S, Mörner T, Samuel WM (2001) Sarcoptes scabiei and Sarcoptic Mange. In: Samuel WM, Pybus MJ, Kocan AA (eds) Parasitic diseases of wild mammals. Iowa State University Press, Ames, pp 107–119
Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102. https://doi.org/10.1016/j.tree.2006.11.001
Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulation. J Comput Graph Stat 7:434–455. https://doi.org/10.1080/10618600.1998.10474787
Catalano S, Lejeune M, Liccioli S et al (2012) Echinococcus multilocularis in urban coyotes, Alberta, Canada. Emerg Infect Dis 18:1625–1628. https://doi.org/10.3201/eid1810.120119
Cypher BL, Rudd JL, Westall TL et al (2017) Sarcoptic mange in endangered kit foxes (Vulpes macrotis mutica): case histories, diagnoses, and implications for conservation. J Wildl Dis 53:46–53. https://doi.org/10.7589/2016-05-098
Cypher BL, Kelly EC, Westall TL, Van Horn Job CL (2018) Coyote diet patterns in the Mojave Desert: implications for threatened desert tortoises. Pacific Conserv Bio 24:44–54. https://doi.org/10.1071/PC17039
da Silva J, Woodroffe R, Macdonald DW (1993) Habitat, food availability and group territoriality in the European badger, Meles meles. Oecologia 95:558–564. https://doi.org/10.1007/bf00317441
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449. https://doi.org/10.1126/science.287.5452.443
Davis AJ, Kirby JD, Chipman RB et al (2019) Not all surveillance data are created equal—a multi-method dynamic occupancy approach to determine rabies elimination from wildlife. J Appl Ecol. https://doi.org/10.1111/1365-2664.13477
Ellington EH, Gehrt SD (2019) Behavioral responses by an apex predator to urbanization. Behav Ecol 30:821–829. https://doi.org/10.1093/beheco/arz019
Gehrt SD, Riley SPD (2010) Coyote (Canis latrans). In: Gehrt SD, Riley SPD, Cypher BL (eds) Urban carnivores: ecology, conflict, and conservation. The Johns Hopkins University Press, Baltimore
Gehrt SD, Anchor C, White LA (2009) Home range and landscape use of coyotes in a metropolitan landscape: conflict or coexistence? J Mammal 90:1045–1057. https://doi.org/10.1644/08-MAMM-A-277.1
Gehrt SD, Riley SPD, Cypher BL (2010) Urban carnivores: ecology, conflict, and conservation. The John Hopkins University Press, Baltimore
Gese EM, Bekoff M (2004) Coyote Canis latrans Say, 1823. In: Sillero-zubiri C, Hoffmann M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs. IUCN, Cambridge, p 443
Grinder MI, Krausman PR (2001) Home range, habitat use, and nocturnal activity of coyotes in an urban environment. J Wildl Manage 65:887–898. https://doi.org/10.2307/3803038
Grubbs SE, Krausman PR (2009) Use of urban landscape by coyotes. Southwest Nat 54:1–12. https://doi.org/10.1894/MLK-05.1
Hayden P (1966) Seasonal occurrence of jackrabbits on jackass flat. Nevada J Wildl Manage 30:835. https://doi.org/10.2307/3798292
Hooten MB, Hobbs NT (2015) A guide to Bayesian model selection for ecologists. Ecol Monogr 85:3–28. https://doi.org/10.1890/14-0661.1
Huebschman JJ, Hoerner SA, White JP et al (2019) Detection of Pseudogymnoascus destructans on Wisconsin bats during summer. J Wildl Dis 55:673–677. https://doi.org/10.7589/2018-06-146
Jones H, Pekins P, Kantar L et al (2019) Mortality assessment of moose (Alces alces) calves during successive years of winter tick (Dermacentor albipictus) epizootics in New Hampshire and Maine (USA). Can J Zool 97:22–30. https://doi.org/10.1139/cjz-2018-0140
Kellner K (2018) jagsUI: a Wrapper Around “rjags” to Streamline “JAGS” Analyses
Kluever BM, Gese EM, Dempsey SJ (2016) Influence of free water availability on a desert carnivore and herbivore. Curr Zool 63:121–129. https://doi.org/10.1093/cz/zow071
MacKenzie DI (2006) Modeling the probability of resource use: the effect of, and dealing with, detecting a species imperfectly. J Wildl Manage 70:367–374. https://doi.org/10.2193/0022-541X(2006)70[367:MTPORU]2.0.CO;2
MacKenzie DI, Nichols JD, Seamans ME, Gutiérrez RJ (2009) Modeling species occurrence dynamics with multiple states and imperfect detection. Ecology 90:823–835. https://doi.org/10.1890/08-0141.1
McClintock BT, Nichols JD, Bailey LL et al (2010) Seeking a second opinion: uncertainty in disease ecology. Ecol Lett 13:659–674. https://doi.org/10.1111/j.1461-0248.2010.01472.x
Montecino-Latorre D, Cypher BL, Rudd JL, Clifford DL, Mazet JAK, Foley JE (2019) Assessing the role of dens in the spread, establishment and persistence of sarcoptic mange in an endangered canid. Epidemics 27:28–40. https://doi.org/10.1016/j.epidem.2019.01.001
Muneza AB, Ortiz-Calo W, Packer C et al (2019) Quantifying the severity of giraffe skin disease via photogrammetry analysis of camera trap data. J Wildl Dis 55:770–781. https://doi.org/10.7589/2018-06-149
Murray M, Edwards MA, Abercrombie B, St. Clair CC (2015) Poor health is associated with use of anthropogenic resources in an urban carnivore. Proc Royal Soc B Biol Sci 282:20150009. https://doi.org/10.1098/rspb.2015.0009
Murray MH, Hill J, Whyte P, St. Clair CC (2016) Urban compost attracts coyotes, contains toxins, and may promote disease in urban-adapted wildlife. EcoHealth 13:285–292. https://doi.org/10.1007/s10393-016-1105-0
Nagy KA, Shoemaker VH, Costa WR (1976) Water, electrolyte, and nitrogen budgets of jackrabbits (Lepus californicus) in the Mojave Desert. Physiol Zool 49:351–363. https://doi.org/10.1086/physzool.49.3.30155693
National Centers for Environmental Information (NCEI) (2020) Climate Data Online: Barstow Daggett Airport, CA US (USW00023161). https://www.ncdc.noaa.gov/cdo-web/datatools/findstation on 23 April 2020
Newman TJ, Baker PJ, Harris S (2002) Nutritional condition and survival of red foxes with sarcoptic mange. Can J Zool 80:154–161. https://doi.org/10.1139/Z01-216
Newsome SD, Garbe HM, Wilson EC, Gehrt SD (2015) Individual variation in anthropogenic resource use in an urban carnivore. Oecologia 178:115–128. https://doi.org/10.1007/s00442-014-3205-2
Nichols JD, Hines JE, MacKenzie DI et al (2007) Occupancy estimation and modeling with multiple states and state uncertainty. Ecology 88:1395–1400. https://doi.org/10.1890/06-1474
Patz JA, Daszak P, Tabor GM et al (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112:1092–1098. https://doi.org/10.1289/ehp.6877
Pence DB, Ueckermann E (2002) Sarcoptic mange in wildlife. Rev Sci Tech 21:385–398. https://doi.org/10.20506/rst.21.2.1335
Pence DB, Windberg LA, Pence BC, Sprowls R (1983) The epizootiology and pathology of sarcoptic mange in coyotes, Canis latrans, from south Texas. J Parasitol 69:1100–1115. https://doi.org/10.2307/3280873
Plowright RK, Foley P, Field HE et al (2011) Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc R Soc B Biol Sci 278:3703–3712. https://doi.org/10.1098/rspb.2011.0522
Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), March 20–22, Vienna, Austria. p ISSN 1609–395X
Preece ND, Abell SE, Grogan L et al (2017) A guide for ecologists: detecting the role of disease in faunal declines and managing population recovery. Biol Conserv 214:136–146. https://doi.org/10.1016/j.biocon.2017.08.014
R Core Team (2018) R: a language and environment for statistical computing. R Development Core Team, Vienna
Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc B Biol Sci 364:37–49. https://doi.org/10.1098/rstb.2008.0184
Reddell CD (2018) Anthropogenic resource use and disease dynamics in a desert coyote population. M.S. thesis, New Mexico State University, Las Cruces, New Mexico
Robinson QH, Bustos D, Roemer GW (2014) The application of occupancy modeling to evaluate intraguild predation in a model carnivore system. Ecology 95:3112–3123. https://doi.org/10.1890/13-1546.1
Rodrigues RA, Massara RL, Bailey LL et al (2020) Using a multistate occupancy approach to determine molecular diagnostic accuracy and factors affecting avian haemosporidian infections. Sci Rep 10:8480. https://doi.org/10.1038/s41598-020-65523-x
Royle JA, Kéry M (2007) A Bayesian state-space formulation of dynamic occupancy models. Ecology 88:1813–1823. https://doi.org/10.1890/06-0669.1
Saito MU, Sonoda Y (2017) Symptomatic raccoon dogs and sarcoptic mange along an urban gradient. EcoHealth 14:318–328. https://doi.org/10.1007/s10393-017-1233-1
Scott DM, Baker R, Charmen N et al (2020) A citizen science based survey method for estimating the density of urban carnivores. PLoS ONE 13:e0197445. https://doi.org/10.1371/journal.pone.0197445
Spiegelhalter DJ, Best NG, Carlin BR, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc Ser B-Statistical Methodol 64:583–616. https://doi.org/10.1111/1467-9868.00353
U.S. Census Bureau (2010) QuickFacts Fort Irwin CDP, California. https://www.census.gov/quickfacts/fortirwincdpcalifornia. Accessed 5 May 2017
Vikøren T, Lillehaug A, Åkerstedt J et al (2008) A severe outbreak of contagious ecthyma (orf) in a free-ranging musk ox (Ovibos moschatus) population in Norway. Vet Microbiol 127:10–20. https://doi.org/10.1016/j.vetmic.2007.07.029
Western Regional Climate Center (WRCC) (2016) Cooperative climatological data summaries: Daggett FAA Airport, California (042257). Retrieved from http://www.wrcc.dri.edu/cgi-bin/cliMAIN.pl?ca2257 on 29 May 2016
Williams ES, Young S (1980) Chronic wasting disease of captive mule deer: a spongiform encephalopathy. J Wildl Dis 16:89–98. https://doi.org/10.7589/0090-3558-16.1.89
Wilson DJ, McFarlane L (2012) Contagious ecthyma in a Rocky Mountain bighorn sheep from Utah. Human-Wildlife Interact 6:7–11. https://doi.org/10.26077/pggv-w922
Woodroffe R, Donnelly CA, Cox DR et al (2009) Bovine tuberculosis in cattle and badgers in localized culling areas. J Wildl Dis 45:128–143. https://doi.org/10.7589/0090-3558-45.1.128
Wright AN, Gompper ME (2005) Altered parasite assemblages in raccoons in response to manipulated resource availability. Oecologia 144:148–156. https://doi.org/10.1007/s00442-005-0018-3
Acknowledgements
We would like to thank the New Mexico State University Agricultural Experiment Station; United States Geological Survey, New Mexico Cooperative Fish and Wildlife Research Unit; NTC Fort Irwin Directorate of Public Works; and the U.S. Army Corps of Engineers: Construction Engineering Research Laboratory for funding. We thank L. Aker, C. Everly, D. Housman, T. Karish, I. Dancourt, and J. Nierman for their field or logistical assistance. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Author information
Authors and Affiliations
Contributions
GWR, JWC, CDR, and FA conceived the study; GWR, JWC and DKD obtained the funding; CDR and DKD collected the data; FA, CDR and GWR performed the analysis and wrote the manuscript; all authors helped interpret the results and provided editorial advice.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
For this type of study formal consent is not required because we only photographed animals and did not handle them. For additional work mentioned here (Reddell 2018), consent for capturing and handling animals was approved by the IACUC of NMSU (Protocol # 2015-001) and the California Department of Fish and Wildlife (Permit # 2330).
Additional information
Communicated by Dan MacNulty.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Reddell, C.D., Abadi, F., Delaney, D.K. et al. Urbanization’s influence on the distribution of mange in a carnivore revealed with multistate occupancy models. Oecologia 195, 105–116 (2021). https://doi.org/10.1007/s00442-020-04803-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04803-9