{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T02:43:26Z","timestamp":1790736206144,"version":"4.1.0"},"reference-count":55,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2019,4,3]],"date-time":"2019-04-03T00:00:00Z","timestamp":1554249600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100000270","name":"Natural Environment Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000270","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,11,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Spatial heterogeneity in susceptibility and exposure to parasites is a common source of confounding variation in disease ecology studies. However, it is not known whether spatial autocorrelation acts on immunity at small scales, within wild animal populations, and whether this predicts spatial patterns in infection. Here we used a well-mixed wild population of individually recognized red deer (Cervus elaphus) inhabiting a heterogeneous landscape to investigate fine-scale spatial patterns of immunity and parasitism. We noninvasively collected 842 fecal samples from 141 females with known ranging behavior over 2 years. We quantified total and helminth-specific mucosal antibodies and counted propagules of three gastrointestinal helminth taxa. These data were analyzed with linear mixed models using the Integrated Nested Laplace Approximation, using a Stochastic Partial Differentiation Equation approach to control for and quantify spatial autocorrelation. We also investigated whether spatial patterns of immunity and parasitism changed seasonally. We discovered substantial spatial heterogeneity in general and helminth-specific antibody levels and parasitism with two helminth taxa, all of which exhibited contrasting seasonal variation in their spatial patterns. Notably, Fasciola hepatica intensity appeared to be strongly influenced by the presence of wet grazing areas, and antibody hotspots did not correlate with distributions of any parasites. Our results suggest that spatial heterogeneity may be an important factor affecting immunity and parasitism in a wide range of study systems. We discuss these findings with regards to the design of sampling regimes and public health interventions, and suggest that disease ecology studies investigate spatial heterogeneity more regularly to enhance their results, even when examining small geographic areas.<\/jats:p>","DOI":"10.1093\/icb\/icz016","type":"journal-article","created":{"date-parts":[[2019,4,2]],"date-time":"2019-04-02T07:15:08Z","timestamp":1554189308000},"page":"1165-1175","source":"Crossref","is-referenced-by-count":52,"title":["The Fine-Scale Landscape of Immunity and Parasitism in a Wild Ungulate Population"],"prefix":"10.1093","volume":"59","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6260-2662","authenticated-orcid":false,"given":"Gregory F","family":"Albery","sequence":"first","affiliation":[{"name":"Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, EH9 3FL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4315-8628","authenticated-orcid":false,"given":"Daniel J","family":"Becker","sequence":"additional","affiliation":[{"name":"Department of Biology, Indiana University, Bloomington, IN 47405, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fiona","family":"Kenyon","sequence":"additional","affiliation":[{"name":"Pentlands Science Park, Moredun Research Institute, Bush Loan, Midlothian EH26 0PZ, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel H","family":"Nussey","sequence":"additional","affiliation":[{"name":"Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, EH9 3FL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josephine M","family":"Pemberton","sequence":"additional","affiliation":[{"name":"Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, EH9 3FL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,4,3]]},"reference":[{"key":"2019111919001780300_icz016-B1","doi-asserted-by":"crossref","first-page":"e2003538.","DOI":"10.1371\/journal.pbio.2003538","article-title":"The ecology of immune state in a wild mammal, Mus musculus domesticus","volume":"16","author":"Abolins","year":"2018","journal-title":"PLoS Biol"},{"key":"2019111919001780300_icz016-B2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0031182018000185","article-title":"Seasonality of helminth infection in wild red deer varies between individuals and between parasite taxa","volume":"145","author":"Albery","year":"2018","journal-title":"Parasitology"},{"key":"2019111919001780300_icz016-B3","article-title":"Reproduction has different costs for immunity and parasitism in a wild mammal","author":"Albery","year":"2018","journal-title":"bioRxiv"},{"key":"2019111919001780300_icz016-B4","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1111\/j.1461-0248.2009.01422.x","article-title":"Regression analysis of spatial data","volume":"13","author":"Beale","year":"2010","journal-title":"Ecol Lett"},{"key":"2019111919001780300_icz016-B5","doi-asserted-by":"crossref","DOI":"10.1098\/rstb.2017.0089","article-title":"Livestock abundance predicts vampire bat demography, immune profiles, and bacterial infection risk","volume":"373","author":"Becker","year":"2018","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"2019111919001780300_icz016-B6","doi-asserted-by":"crossref","DOI":"10.1093\/icb\/icz007","article-title":"Leukocyte profiles reflect geographic range limits in a widespread Neotropical bat","author":"Becker","year":"2019","journal-title":"Integr Comp Biol"},{"key":"2019111919001780300_icz016-B7","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1111\/tbed.12682","article-title":"Fasciola and fasciolosis in ruminants in Europe: identifying research needs","volume":"65","author":"Beesley","year":"2018","journal-title":"Transbound Emerg Dis"},{"key":"2019111919001780300_icz016-B8","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.ijpara.2016.09.007","article-title":"Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance","volume":"47","author":"Beesley","year":"2017","journal-title":"Int J Parasitol"},{"key":"2019111919001780300_icz016-B9","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1080\/00288233.1992.10417701","article-title":"Heritability of and genetic correlations among faecal egg counts and productivity traits in Romney sheep","volume":"35","author":"Bisset","year":"1992","journal-title":"NZ J Agric Res"},{"key":"2019111919001780300_icz016-B10","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.tvjl.2006.11.003","article-title":"Wild deer as a source of infection for livestock and humans in the UK","volume":"174","author":"Bohm","year":"2007","journal-title":"Vet J"},{"key":"2019111919001780300_icz016-B11","doi-asserted-by":"crossref","first-page":"301","DOI":"10.14202\/vetworld.2015.301-315","article-title":"Tick-borne infections in human and animal population worldwide","volume":"8","author":"Brites-Neto","year":"2015","journal-title":"Vet World"},{"key":"2019111919001780300_icz016-B12","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1016\/j.ijpara.2006.05.009","article-title":"Contrasting patterns in the small-scale heterogeneity of human helminth infections in urban and rural environments in Brazil","volume":"36","author":"Brooker","year":"2006","journal-title":"Int J Parasitol"},{"key":"2019111919001780300_icz016-B13","first-page":"1","article-title":"Variation and covariation in strongyle infection in East African shorthorn zebu calves","volume":"142","author":"Callaby","year":"2014","journal-title":"Parasitology"},{"key":"2019111919001780300_icz016-B14","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1017\/S0031182013001972","article-title":"A brief review of spatial analysis concepts and tools used for mapping, containment and risk modelling of infectious diseases and other illnesses","volume":"141","author":"Caprarelli","year":"2014","journal-title":"Parasitology"},{"key":"2019111919001780300_icz016-B15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-017-13686-5","article-title":"Immunosenescence patterns differ between populations but not between sexes in a long-lived mammal","volume":"7","author":"Cheynel","year":"2017","journal-title":"Sci Rep"},{"key":"2019111919001780300_icz016-B16","doi-asserted-by":"crossref","first-page":"20132985.","DOI":"10.1098\/rspb.2013.2985","article-title":"Wild deer as potential vectors of anthelmintic-resistant abomasal nematodes between cattle and sheep farms","volume":"281","author":"Chintoan-Uta","year":"2014","journal-title":"Proc R Soc B"},{"key":"2019111919001780300_icz016-B17","author":"Clutton-Brock","year":"1982"},{"key":"2019111919001780300_icz016-B18","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1139\/cjfas-2014-0159","article-title":"Applying Bayesian spatiotemporal models to fisheries bycatch in the Canadian Arctic","volume":"72","author":"Cosandey-Godin","year":"2015","journal-title":"Can J Fish Aquat Sci"},{"key":"2019111919001780300_icz016-B19","doi-asserted-by":"crossref","first-page":"852.","DOI":"10.1890\/0012-9658(1997)078[0852:PSLDAC]2.0.CO;2","article-title":"Population substructure, local density, and calf winter survival in red deer (Cervus elaphus)","volume":"78","author":"Coulson","year":"1997","journal-title":"Ecology"},{"key":"2019111919001780300_icz016-B20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0125586","article-title":"Investment in constitutive immune function by North American elk experimentally maintained at two different population densities","volume":"10","author":"Downs","year":"2015","journal-title":"PLoS One"},{"key":"2019111919001780300_icz016-B21","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.cobeha.2016.09.006","article-title":"Group living and pathogen infection revisited","volume":"12","author":"Ezenwa","year":"2016","journal-title":"Curr Opin Behav Sci"},{"key":"2019111919001780300_icz016-B22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0162420","article-title":"Prevalence of liver fluke (Fasciola hepatica) in wild red deer (Cervus elaphus): coproantigen ELISA is a practicable alternative to faecal egg counting for surveillance in remote populations","volume":"11","author":"French","year":"2016","journal-title":"PLoS ONE"},{"key":"2019111919001780300_icz016-B23","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1111\/ele.12965","article-title":"Declining home range area predicts reduced late-life survival in two wild ungulate populations","volume":"21","author":"Froy","year":"2018","journal-title":"Ecol Lett"},{"key":"2019111919001780300_icz016-B24","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1098\/rsif.2007.1019","article-title":"Impact of scale on the effectiveness of disease control strategies for epidemics with cryptic infection in a dynamical landscape: an example for a crop disease","volume":"4","author":"Gilligan","year":"2007","journal-title":"J R Soc Interface"},{"key":"2019111919001780300_icz016-B25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1365-2699.2011.02637.x","article-title":"Eight (and a half) deadly sins of spatial analysis","volume":"39","author":"Hawkins","year":"2012","journal-title":"J Biogeogr"},{"key":"2019111919001780300_icz016-B26","doi-asserted-by":"crossref","first-page":"S58","DOI":"10.1086\/676929","article-title":"Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics","volume":"184(Suppl.)","author":"Hayward","year":"2014","journal-title":"Am Nat"},{"key":"2019111919001780300_icz016-B27","doi-asserted-by":"crossref","first-page":"3585","DOI":"10.1073\/pnas.1518046113","article-title":"Inbreeding depression across the lifespan in a wild mammal population","volume":"113","author":"Huisman","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2019111919001780300_icz016-B28","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1111\/pim.12153","article-title":"Beyond mice and men: environmental change, immunity and infections in wild ungulates","volume":"37","author":"Jolles","year":"2015","journal-title":"Parasite Immunol"},{"key":"2019111919001780300_icz016-B29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fvets.2018.00090","article-title":"The certainty of uncertainty: potential sources of bias and imprecision in disease ecology studies","volume":"5","author":"Lachish","year":"2018","journal-title":"Front Vet Sci"},{"key":"2019111919001780300_icz016-B30","doi-asserted-by":"crossref","first-page":"9699","DOI":"10.1002\/ece3.3506","article-title":"Responses to a warming world: integrating life history, immune investment, and pathogen resistance in a model insect species","volume":"7","author":"Laughton","year":"2017","journal-title":"Ecol Evol"},{"key":"2019111919001780300_icz016-B31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v063.i19","article-title":"Bayesian spatial modelling with R-INLA","volume":"63","author":"Lindgren","year":"2015","journal-title":"J Stat Softw"},{"key":"2019111919001780300_icz016-B32","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1111\/j.1467-9868.2011.00777.x","article-title":"An explicit link between Gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach","volume":"73","author":"Lindgren","year":"2011","journal-title":"J R Stat Soc B"},{"key":"2019111919001780300_icz016-B33","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.csda.2013.04.014","article-title":"Bayesian computing with INLA: new features","volume":"67","author":"Martins","year":"2013","journal-title":"Comput Stat Data Anal"},{"key":"2019111919001780300_icz016-B34","first-page":"3","article-title":"Elaphostrongylus cervi\u2014a review","volume":"16","author":"Mason","year":"1989","journal-title":"Surveillance"},{"key":"2019111919001780300_icz016-B35","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1098\/rspb.2006.3486","article-title":"Lifetime reproductive success and density-dependent, multi-variable resource selection","volume":"273","author":"McLoughlin","year":"2006","journal-title":"Proc R Soc B Biol Sci"},{"key":"2019111919001780300_icz016-B36","doi-asserted-by":"crossref","first-page":"e0005640.","DOI":"10.1371\/journal.pntd.0005640","article-title":"Fine-scale variation in microclimate across an urban landscape changes the capacity of Aedes albopictus to vector arbovirus","volume":"11","author":"Murdock","year":"2017","journal-title":"PLoS Negl Trop Dis"},{"key":"2019111919001780300_icz016-B37","doi-asserted-by":"crossref","first-page":"1411","DOI":"10.1111\/ecog.03625","article-title":"Pathogeography: leveraging the biogeography of human infectious diseases for global health management","volume":"41","author":"Murray","year":"2018","journal-title":"Ecography"},{"key":"2019111919001780300_icz016-B38","doi-asserted-by":"crossref","first-page":"52","DOI":"10.2193\/2007-317","article-title":"Sampling considerations for disease surveillance in wildlife populations","volume":"72","author":"Nusser","year":"2008","journal-title":"J Wildl Manage"},{"key":"2019111919001780300_icz016-B39","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/S0065-308X(08)60437-6","article-title":"Meteorological factors and forecasts of helminthic disease","volume":"7","author":"Ollerenshaw","year":"1969","journal-title":"Adv Parasitol"},{"key":"2019111919001780300_icz016-B40","doi-asserted-by":"crossref","first-page":"160.","DOI":"10.1186\/s13071-015-0773-x","article-title":"Prevalence, risk factors and spatial analysis of liver fluke infections in Danish cattle herds","volume":"8","author":"Olsen","year":"2015","journal-title":"Parasit Vectors"},{"key":"2019111919001780300_icz016-B41","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.tree.2005.03.009","article-title":"Spatial epidemiology: an emerging (or re-emerging) discipline","volume":"20","author":"Ostfeld","year":"2005","journal-title":"Trends Ecol Evol"},{"key":"2019111919001780300_icz016-B42","doi-asserted-by":"crossref","first-page":"5804","DOI":"10.1128\/AEM.00997-15","article-title":"Spatial variation and survival of Salmonella enterica subspecies in a population of Australian sleepy lizards (Tiliqua rugosa)","volume":"81","author":"Parsons","year":"2015","journal-title":"Appl Environ Microbiol"},{"key":"2019111919001780300_icz016-B43","author":"Pawley","year":"2018"},{"key":"2019111919001780300_icz016-B44","doi-asserted-by":"crossref","DOI":"10.1186\/s13071-016-1825-6","article-title":"The influence of red deer space use on the distribution of Ixodes ricinus ticks in the landscape","volume":"9","author":"Qviller","year":"2016","journal-title":"Parasit Vectors"},{"key":"2019111919001780300_icz016-B45","volume-title":"R: a language and environment for statistical computing.","author":"R Core Team","year":"2018"},{"key":"2019111919001780300_icz016-B46","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1111\/j.1467-9868.2008.00700.x","article-title":"Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations","volume":"71","author":"Rue","year":"2009","journal-title":"R Stat Soc"},{"key":"2019111919001780300_icz016-B47","doi-asserted-by":"crossref","first-page":"2466","DOI":"10.1002\/ece3.1533","article-title":"Interactions between density, home range behaviors, and contact rates in the Channel Island fox (Urocyon littoralis)","volume":"5","author":"Sanchez","year":"2015","journal-title":"Ecol Evol"},{"key":"2019111919001780300_icz016-B48","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1111\/j.1600-0587.2000.tb00286.x","article-title":"Geographical variation in blood parasites in feral pigeons: the role of vectors","volume":"23","author":"Sol","year":"2011","journal-title":"Ecography"},{"key":"2019111919001780300_icz016-B49","doi-asserted-by":"crossref","first-page":"2411","DOI":"10.1111\/j.1558-5646.2012.01620.x","article-title":"Shared spatial effects on quantitative genetic parameters: accounting for spatial autocorrelation and home range overlap reduces estimates of heritability in wild red deer","volume":"66","author":"Stopher","year":"2012","journal-title":"Evolution (NY)"},{"key":"2019111919001780300_icz016-B50","first-page":"761","author":"Taylor","year":"2016"},{"key":"2019111919001780300_icz016-B51","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.pt.2009.11.001","article-title":"Can parasites really reveal environmental impact?","volume":"26","author":"Vidal-Mart\u00ednez","year":"2010","journal-title":"Trends Parasitol"},{"key":"2019111919001780300_icz016-B52","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1002\/ece3.1858","article-title":"Fecal antibody levels as a noninvasive method for measuring immunity to gastrointestinal nematodes in ecological studies","volume":"6","author":"Watt","year":"2016","journal-title":"Ecol Evol"},{"key":"2019111919001780300_icz016-B53","first-page":"113","volume-title":"Soay sheep: dynamics and selection in an island population","author":"Wilson","year":"2004"},{"key":"2019111919001780300_icz016-B54","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.tree.2012.10.011","article-title":"Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission","volume":"28","author":"Wood","year":"2013","journal-title":"Trends Ecol Evol"},{"key":"2019111919001780300_icz016-B55","author":"Zuur","year":"2017"}],"container-title":["Integrative and Comparative Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/icb\/article-pdf\/59\/5\/1165\/30989692\/icz016.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/icb\/article-pdf\/59\/5\/1165\/30989692\/icz016.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,11,19]],"date-time":"2019-11-19T19:00:46Z","timestamp":1574190046000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/icb\/article\/59\/5\/1165\/5426770"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,4,3]]},"references-count":55,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2019,4,3]]},"published-print":{"date-parts":[[2019,11,1]]}},"URL":"https:\/\/doi.org\/10.1093\/icb\/icz016","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/483073","asserted-by":"object"}]},"ISSN":["1540-7063","1557-7023"],"issn-type":[{"value":"1540-7063","type":"print"},{"value":"1557-7023","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,11]]},"published":{"date-parts":[[2019,4,3]]}}}