Abstract
Land use change can alter the ecological mechanisms that influence infectious disease exposure in animal populations. However, few studies have empirically integrated the environmental, spatial, and dietary patterns of wildlife epidemiology. We investigate how urbanization, habitat type, and dietary behavior are associated with coyote (Canis latrans) parasitism structure along a gradient of rural to urban land cover using multivariate redundancy analyses. Coyote fecal samples were collected in eight urban and six rural sites in Calgary, Alberta, Canada. Parasite and diet components were identified using common flotation procedures and fecal dietary analysis, respectively. Redundancy analysis was used to identify the best land cover, connectivity, and dietary predictors. We tested for significance using multiple permutation tests and ANOVAs. Significant factors affecting enteric parasite prevalence included dietary and land cover factors (R 2 = 0.4130, P < 0.05). Variation in dietary behavior was observed between urban and rural sites (R 2 = 0.4712, P < 0.05), as anthropogenic diet items (i.e., garbage, crabapples) were strongly influenced by urbanization. Our research supports that developed habitat, grassland cover, and dietary choice interact to possibly influence the exposure of coyote hosts to enteric parasites and pioneers future investigation of disease ecology for natural populations in anthropogenic landscapes.
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Acknowledgements
The authors would like to thank the City of Calgary; Spatial and Numeric Data Services (SANDS), at the University of Calgary for spatial data. We would like to thank the Department of Geography, University of Calgary, NSERC, the Alberta Conservation Association for funding of this research. We would especially like to thank the Sandy Cross Conservation Area, Hamish Kerfoot, Big Hill Springs Provincial Park, the Inglewood Bird Sanctuary, and Fish Creek Provincial Park for the allowance of sampling on their land. We further thank Dr. Susan Kutz for the use of laboratory equipment and expertise for parasitological investigation.
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Appendices
Appendix A: Detailed Description of Methods
Site Selection and Sampling
Sites were chosen based on known coyote occupancy to maximize opportunistic sampling yield, while representing habitat differences. A preliminary investigation of sites verified the presence of coyote feces by walking all sites in a grid-like pattern along transects ranging from 1–4 km transects. We observed diminishing yields of fecal samples beyond ~1 km sampling distances in high defection areas. Sampling was, therefore, standardized by surveying a fixed 1 km transect per site, consisting of defined paths and roads known by preliminary observation to be common defecation sites to maximize sample yields per site. Edges of each transect were chosen at a minimum distance of 4 km from other transects in alternative sampling sites derived by an average maximum reported home ranges of coyotes in North American cities. Because individual coyotes were not being tracked or followed, it was assumed that these transects were common defecation areas for local, independent coyote subpopulations.
Laboratory Analyses
We used a double-centrifugation fecal flotation, a common method in carnivore fecal parasitism surveys. While this method can be unreliable for some canid parasite species, such as specific Taenia spp. and Echinococcus spp., we considered this method satisfactory for our objectives because we identified morphologically indistinguishable parasites to the genus-level instead of species-level, assuming that environmental and host associations with parasite groups are similar. We performed preliminary sensitivity analyses of the flotation method to consider the sensitivity of egg oocyst recovery and identification using 2, 4, and 6 g of feces per sample. Multiple flotations were performed on individual samples to address within-sample parasite detectability. In both preliminary analyses, no differences were observed in the detectability of parasite presence/absence at the genus level. Therefore, a total of 4 g of feces were extracted from equally distributed cross sections of each fecal sample and homogenized before centrifugation and multiple microscope slides were prepared per homogenized sample.
Dietary components were identified using a point-frame method. Hairs and bones were classified to the lowest observable taxonomic level (Kennedy and Carbyn 1981) and then aggregated by dietary category (e.g., small mammals, plants, etc.) for analysis. Insects and birds were identified to order, based on exoskeleton remains and feather barbules. Vegetation and anthropogenic items were identified by morphological characteristics, using a dissection microscope. Percent by volume was measured for each dietary component on a 2.5 cm grid.
Tests of Normality
We tested for multivariate homogeneity using permutation tests of observed parasite and diet observations, including beta-adjusted pairwise distances to account for small sample sizes (Anderson 2006, Gijbels and Omelka 2013). No significance was identified among sites for parasitism (P = 0.583) and diet (P = 0.619) suggesting normality among observed prevalence and relative abundance data, respectively. We performed a second test of normality by skewness (P = 0.89) and kurtosis (P = 0.12) using Mardia’s multivariate normality test (Korkmaz and Goksuluk 2014), where parasite prevalence and dietary relative abundances were suggested to be normally distributed.
Multivariate Parameter Selection
We used a constrained canonical ordination method (redundancy analysis RDA; Legendre and Legendre 2012) to explain the variation in coyote enteric parasite prevalence. For parsimony, we limited redundancy models to five predictors (Legendre and Legendre 2012). Before the RDA analyses were performed, we selected the predictors by ranking models using the Leaps library in R (R Development Core Team 2011). Based on the adjusted R 2 values, we kept the top five variables (Peres-Neto et al. 2006). We chose our top RDA models according to (a) overall model significance, (b) significance of axes 1 and 2, (c) significance of at least two of five predictors; and (d) ecological significance to our study system.
Appendix B
See Figure 4
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Watts, A.G., Lukasik, V.M., Fortin, MJ. et al. Urbanization, Grassland, and Diet Influence Coyote (Canis latrans) Parasitism Structure. EcoHealth 12, 645–659 (2015). https://doi.org/10.1007/s10393-015-1040-5
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DOI: https://doi.org/10.1007/s10393-015-1040-5