Friday, March 01, 2013

Evaluating Spatial Overlap and Relatedness of White-tailed Deer in a Chronic Wasting Disease Management Zone

 
Research Article
 
 
Evaluating Spatial Overlap and Relatedness of White-tailed Deer in a Chronic Wasting Disease Management Zone
 
 
Seth B. Magle mail, * E-mail: SMagle@lpzoo.org
Affiliation: Urban Wildlife Institute, Lincoln Park Zoo, Chicago, Illinois, United States of America
X Michael D. Samuel, Affiliation: U.S. Geological Survey, Wisconsin Cooperative Wildlife Research Unit, University of Wisconsin, Madison, Wisconsin, United States of America
X Timothy R. Van Deelen, Affiliation: Department of Forest and Wildlife Ecology, University of Wisconsin, Madison, Wisconsin, United States of America
X Stacie J. Robinson, Affiliation: Department of Forest and Wildlife Ecology, University of Wisconsin, Madison, Wisconsin, United States of America
 
 
X Nancy E. Mathews
 
 
 
Abstract
 
 
Wildlife disease transmission, at a local scale, can occur from interactions between infected and susceptible conspecifics or from a contaminated environment. Thus, the degree of spatial overlap and rate of contact among deer is likely to impact both direct and indirect transmission of infectious diseases such chronic wasting disease (CWD) or bovine tuberculosis. We identified a strong relationship between degree of spatial overlap (volume of intersection) and genetic relatedness for female white-tailed deer in Wisconsin’s area of highest CWD prevalence. We used volume of intersection as a surrogate for contact rates between deer and concluded that related deer are more likely to have contact, which may drive disease transmission dynamics. In addition, we found that age of deer influences overlap, with fawns exhibiting the highest degree of overlap with other deer. Our results further support the finding that female social groups have higher contact among related deer which can result in transmission of infectious diseases. We suggest that control of large social groups comprised of closely related deer may be an effective strategy in slowing the transmission of infectious pathogens, and CWD in particular.
 
 
snip...
 
 
Discussion
 
 
Social interactions, as well as group membership, may influence transmission of wildlife diseases [1], [2] and relatedness may be more important for transmission than simple proximity [21]. However, proximity can be a poor surrogate for relatedness [14] or group membership [6]. While related female white-tailed deer form social clusters on the landscape [9], [21], [44], social groups may overlap in space, but not in time. Thus, proximity of deer alone is not enough to discern relatedness, and by extension, the likelihood of transmission of infectious diseases [21]. Even adult females and fawns trapped in the same location are not always mother-offspring pairs [45]. The mechanisms by which related deer transmit infectious disease to one another are unclear, however. Because volume of intersection is a useful predictor of both direct and indirect contact rates in deer [6], it appears that related deer are more likely to come into contact, and therefore drive the dynamics of infectious diseases [21]. We identified a clear relationship between overlap (as measured by a volume of intersection) and relatedness for white-tailed deer in south-central Wisconsin. In addition, we found that age of deer influenced degree of overlap, with adult-fawn, yearling-fawn, and fawn-fawn pairs overlapping more strongly, whereas adult-adult pairs, and adult-yearling and yearling-yearling pairs exhibited lower overlap. Kinship categories were stronger predictors than continuous Rxy values, suggesting that deer beyond a certain degree of relatedness exhibit higher amounts of overlap. Even within kinship classifications, such as half-siblings or parent and offspring, there is variation in the proportion of shared DNA, and thus degree of relatedness may be less important than the nature of the social relationship between individual deer (e.g., parent offspring vs. cousins).
 
 
We found that first order kin had 32.5 times as much overlap as unrelated deer. This value is somewhat larger than a previous finding that deer in Illinois had 5.0–22.1 times greater odds of direct contact when they belonged to the same social group, as estimated by proximity [6]. However, our results may be closer to a separate study in Wisconsin indicating that deer were >100 times more likely to become infected with CWD when a highly related infected female was in close proximity, with much lower effects from proximal unrelated animals [21]. This indicates that probability of CWD infection is likely higher among closely related deer, because they have much higher contact rates, as opposed to unrelated deer that simply share space, but have lower contact rates. In addition, a higher probability of transmission may occur because of the more intense nature of contacts among related deer [46], [47]. Previous observational studies indicate that parent-offspring pairs engage in significant contact during the first year of life [46]. Studies that investigate the spatial dynamics of disease transmission in wild populations should include direct observation of deer behavior to more thoroughly address the heterogeneous disease transmission that result from the social structure of deer [22].
 
 
Our finding that adult-fawn pairs had higher overlap is not surprising given patterns of maternal care in white-tailed deer [8]. The average VI of probable parent-offspring pairs (adult-fawn pairs with Rxy values >0.5) were very high (0.64 in datasetadult, 0.55 in datasetcapgroup), compared to the overall mean (0.22 in datasetadult, 0.20 in datasetcapgroup). Adult-fawn pairs with moderate relatedness value (0.26< Rxy <0 .5="" 0.22="" 0.36="" adult="" and="" approximating="" between="" breed="" datasetadult="" datasetcapgroup="" deer.="" disperse="" div="" establish="" exhibited="" explain="" females="" from="" had="" help="" home="" however="" in="" low="" lower="" may="" mean="" mother="" natal="" of="" on="" once="" overall="" overlap="" pairs="" periphery="" range="" ranges="" rarely="" reduced="" relatedness="" respectively="" s="" slightly="" sometimes="" system="" the="" their="" they="" this="" those="" values="" vi="" which="" with="" xy="" yearling="">
 
 
Female white-tailed deer are highly philopatric, characterized by stable home ranges with a high degree of overlap among individuals within social groups [6], [9], [44], [46]. However, social structure of deer is less typical where rates of harvest are high and age structure is biased towards young animals [14], [48]. Nonetheless, we found that overlap (as measured by VI) closely associated with degree of relatedness, providing evidence for social structure at a local scale in spite of heavy harvest pressure. While ongoing disease eradication efforts may have temporarily increased deer harvest, this population has been subjected to ongoing harvest for many years, and CWD control efforts are unlikely to have produced the patterns observed. The strong matriarchal social structure of female white-tailed deer likely prevents homogenous mixing of individuals [6], [9] and homogeneous CWD transmission among members of different social groups [21].
 
 
The degree to which deer contact each another varies seasonally [6, 56]. However, to ensure sufficient observations, our analyses were based on annual data and provide no insight into seasonal patterns. In addition to relatedness, hotspots of activity such as scrapes, rubs, feeding/baiting sites, and mineral licks also likely play a role in contact rates of cervids and potential disease transmission [49], [50], [51]. We did not identify such features in our study and have no basis to evaluate the contribution of these behavioral hotspots to potential transmission of disease. Deer may also be more likely to overlap in agricultural areas due to concentrated food sources [3], [16], [25], [52]. In fragmented systems, deer would likely congregate closely in areas of remaining resources, particularly in seasons when food is limited [52]. Unfortunately, accuracy of the spatial locations in this study was insufficient to investigate the effects of habitat use, given that the study area is a complex mosaic of forested and agricultural land [25]. Our study focused on female deer because they are most often targeted for population control and, unlike males, rarely engage in long-distance movements [9], [21], [25]. However, males are more frequently CWD positive than females (Grear et al. 2006), and long-distance movements by males may be important in the geographic spread of CWD.
 
 
CWD can be transmitted both directly (by deer-to-deer contact) and indirectly (via contamination of the environment), though the importance of these modes of transmission in the wild are unknown [17], [19], [21]. VI provides a metric for both direct and indirect contact, though the spatial-temporal resolution of our data is insufficient to differentiate these specific events. While it is possible for two deer who overlap in space to avoid direct contact, indirect contact is virtually guaranteed, particularly given the likely occurrence of congregation points such as scrapes, rubs, feeding/baiting sites, and mineral licks. However, given previous findings that contact rates vary predictably with VI [6], we believe our findings likely apply for both direct and indirect transmission scenarios. Our findings support previous research that suggest CWD should spread more rapidly among related deer [21]. As such, control of large related social groups may be an effective strategy in slowing pathogen transmission, particularly given that there is little evidence that female harvest impacts movement behavior [16]. We also found limited overlap among unrelated deer, suggesting that disease spread among social groups, which is needed to sustain disease, may occur between neighboring social groups. We believe the rate and mechanisms of disease transmission between adjacent social groups is an important area for future research.
 
 
We provide an important step in understanding the mechanisms underlying observed patterns of CWD transmission, namely, that related individuals are more likely to come into close proximity on the landscape, where disease transmission may occur either directly or indirectly. Further progress in understanding the specifics of disease spread will be necessary to devise practical strategies for deer management.
Citation: Magle SB, Samuel MD, Van Deelen TR, Robinson SJ, Mathews NE (2013) Evaluating Spatial Overlap and Relatedness of White-tailed Deer in a Chronic Wasting Disease Management Zone. PLoS ONE 8(2): e56568. doi:10.1371/journal.pone.0056568
 
 
Editor: Justin David Brown, University of Georgia, United States of America
 
Received: October 5, 2012; Accepted: January 14, 2013; Published: February 20, 2013
 
 
Copyright: © 2013 Magle et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
 
 
Funding: This project was supported by the Wisconsin Department of Natural Resources, Whitetails Unlimited, the University of Wisconsin, the National Beef and Cattleman’s Association, and the North Central Agricultural Experiment Station Hatch Program. Thanks to the University of Wisconsin’s Department of Forest & Wildlife Ecology and the Nelson Institute for Environmental Studies for assistance with publication costs. Note that any use of trade, product or firm names is for descriptive purposes, and does not imply endorsement by the United States Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
 
 
Competing interests: The authors have declared that no competing interests exist.
 






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