Abstract
Incorporating host behavioral variation into epidemiological models is important for predicting host-pathogen dynamics. Animals living at high densities or with many strong social connections are predicted to have greater risk of acquiring pathogens. Using social network analysis, we tested the hypothesis that variation in the strength of social connections would influence simulated elk (Cervus canadensis) pathogen dynamics. We quantified fine-scale social connections for captive elk at three experimentally manipulated densities and wild elk at two natural densities. We applied susceptible-infected epidemiological models to networks to infer the relationship between fine-scale host sociality and simulated pathogen dynamics. Networks were filtered based on four association thresholds to determine how variation in the strength of social connections influenced pathogen dynamics. Our simulations suggest that social behavior interacts with population density to predict pathogen dynamics, but this effect was sex-specific. For both males and females at higher density, elk had strong social connections, resulting in higher number of infected individuals. We observed differences in social connections across density, and these results translated to our simulations, which predicted density-dependent pathogen dynamics for captive and wild elk networks. Our results highlight host social behavior as a potential mechanism driving variation in the relationship between population density and pathogen dynamics. Elk are reservoir hosts for numerous emerging infectious diseases, and our models suggest that density-dependent host social behavior could influence pathogen dynamics in elk social networks.
Significance statement
Animal population density can influence transmission of parasites and pathogens, but variation in social connections at different densities could impact this relationship. Using social network analysis and epidemiological simulations, we tested the hypothesis that density-dependent variation in social connections would influence pathogen dynamics using captive and free-ranging populations of elk (Cervus elaphus). For all elk groups, simulated number of infected individuals increased with social connectedness. In addition, our simulations suggest that social connectedness interacts with population density to predict number of infected individuals, but this effect was sex-specific. For males and females at high density, elk had strong social connections, resulting in more infected individuals; this relationship was linear for males and non-linear for females. Taken together, our results suggest fine-scale measures of social behavior vary with population density, a result which could have implications for pathogen dynamics.
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References
Altizer S, Nunn C, Thrall P et al (2003) Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annu Rev Ecol Evol S 34:517–547. https://doi.org/10.1146/annurev.ecolsys.34.030102.151725
Bateman AW, Ozgul A, Coulson T, Clutton-Brock TH (2012) Density dependence in group dynamics of a highly social mongoose, Suricata suricatta. J Anim Ecol 81:628–639. https://doi.org/10.1111/j.1365-2656.2011.01934.x
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Böhm M, Palphramand KL, Newton-Cross G, Hutchings MR, White PCL (2008) Dynamic interactions among badgers: implications for sociality and disease transmission. J Anim Ecol 77:735–745. https://doi.org/10.1111/j.1365-2656.2007.0
Borremans B, Reijniers J, Hughes NK, Godfrey SS, Gryseels S, Makundi RH, Leirs H (2017) Nonlinear scaling of foraging contacts with rodent population density. Oikos 126:792–800. https://doi.org/10.1111/oik.03623
Boyland NK, James R, Mlynski DT, Madden JR, Croft DP (2013) Spatial proximity loggers for recording animal social networks: consequences of inter-logger variation in performance. Behav Ecol Sociobiol 67:1877–1890. https://doi.org/10.1007/s00265-013-1622-6
Brook RK, Vander Wal E, van Beest FM, McLachlan SM (2013) Evaluating use of cattle winter feeding areas by elk and white-tailed deer: implications for managing bovine tuberculosis transmission risk from the ground up. Prev Vet Med 108:137–147. https://doi.org/10.1016/j.prevetmed.2012.07.017
Cattet MRL, Caulkett NA, Wilson C, Vandenbrink T, Brook RK (2004) Intranasal administration of xylazine to reduce stress in elk captured by net gun. J Wildl Dis 40:562–565. https://doi.org/10.7589/0090-3558-40.3.562
Conner MM, Ebinger MR, Blanchong JA, Cross PC (2008) Infectious disease in cervids of North America: data, models, and management challenges. Ann N Y Acad Sci 1134:146–172. https://doi.org/10.1196/annals.1439.005
Cote IM, Poulin R (1995) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165
Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507. https://doi.org/10.1016/j.tree.2011.05.012
Cross PC, Creech TG, Ebinger MR, Manlove K, Irvine K, Henningsen J, Rogerson J, Scurlock BM, Creel S (2013) Female elk contacts are neither frequency nor density dependent. Ecology 94:2076–2086. https://doi.org/10.1890/12-2086.1
Cross PC, Heisey DM, Scurlock BM, Edwards WH, Ebinger MR, Brennan A (2010) Mapping brucellosis increases relative to elk density using hierarchical bayesian models. PLoS One 5:e10322. https://doi.org/10.1371/journal.pone.0010322
Cross PC, Lloyd-Smith JO, Johnson PLF, Getz W (2005) Duelling timescales of host movement and disease recovery determine invasion of disease in structured populations. Ecol Lett 8:587–595. https://doi.org/10.1111/j.1461-0248.2005.00760.x
Csárdi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Syst 1695:1–9
Donnelly CA, Woodroffe R, Cox DR, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Wei G, Gettinby G, Gilks P, Jenkins H, Johnston WT, le Fevre AM, McInerney JP, Morrison WI (2006) Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439:843–846. https://doi.org/10.1038/nature04454
Drewe JA (2010) Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proc R Soc Lond B 277:633–642. https://doi.org/10.1098/rspb.2009.1775
Ezenwa VO, Ghai RR, Mckay AF, Williams AE (2016) Group living and pathogen infection revisited. Curr Opin Behav Sci 12:66–72. https://doi.org/10.1016/j.cobeha.2016.09.006
Farine DR (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320. https://doi.org/10.1111/2041-210X.12772
Farine DR, Whitehead H (2015) Constructing, conducting and interpreting animal social network analysis. J Anim Ecol 84:1144–1163. https://doi.org/10.1111/1365-2656.12418
Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7:88–94. https://doi.org/10.1046/j.1461-0248.2003.00552.x
Ferrari N, Rosà R, Lanfranchi P, Ruckstuhl KE (2010) Effect of sexual segregation on host-parasite interaction: model simulation for abomasal parasite dynamics in alpine ibex (Capra ibex). Int J Parasitol 40:1285–1293. https://doi.org/10.1016/j.ijpara.2010.03.015
Fowler CW (1981) Density dependence as related to life history strategy. Ecology 62:602–610
Hawley DM, Etienne RS, Ezenwa VO, Jolles AE (2011) Does animal behavior underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integr Comp Biol 51:528–539. https://doi.org/10.1093/icb/icr062
Hebblewhite M, Pletscher DH (2002) Effects of elk group size on predation by wolves. Can J Zool 80:800–809. https://doi.org/10.1139/z02-059
Hirsch BT, Prange S, Hauver SA, Gehrt SD (2013) Raccoon social networks and the potential for disease transmission. PLoS One 8:e75830. https://doi.org/10.1371/journal.pone.0075830
Hopkins SR, Fleming-Davies AE, Belden LK, Wojdak JM (2020) Systematic review of modeling assumptions and empirical evidence: does parasite transmission increase contly with host density? Methods Ecol Evol 11:476–486. https://doi.org/10.1111/2041-210x.13361
James R, Croft DP, Krause J (2009) Potential banana skins in animal social network analysis. Behav Ecol Sociobiol 63:989–997. https://doi.org/10.1007/s00265-009-0742-5
Jolles AE, Ezenwa VO (2015) Ungulates as model systems for the study of disease processes in natural populations. J Mammal 96:4–15. https://doi.org/10.1093/jmammal/gyu007
Krause S, Wilson ADM, Ramnarine IW, Herbert-Read JE, Clément RJG, Krause J (2017) Guppies occupy consistent positions in social networks: mechanisms and consequences. Behav Ecol 28:429–438. https://doi.org/10.1093/beheco/arw177
Lachish S, McCallum H, Mann D, Pukk CE, Jones ME (2010) Evaluation of selective culling of infected individuals to control tasmanian devil facial tumor disease. Conserv Biol 24:841–851. https://doi.org/10.1111/j.1523-1739.2009.01429.x
Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335
Long RA, Rachlow JL, Kie JG (2009) Sex-specific responses of North American elk to habitat manipulation. J Mammal 90:423–432. https://doi.org/10.1644/08-MAMM-A-181.1
Manlove K, Cassirer EF, Cross P, Plowright RK, Hudson PJ (2014) Costs and benefits of group living with disease: a case tudy of pneumonia in bighorn lambs (Ovis canadensis). Proc R Soc B 281:20142331
McCallum H (2008) Tasmanian devil facial tumour disease: lessons for conservation biology. Trends Ecol Evol 23:631–637. https://doi.org/10.1016/j.tree.2008.07.001
McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16:295–300
Mereszczak IM, Krueger WC, Vavra M (1981) Effects of ruminant digestion on germination of Lehmann love-grass seed. J Range Manag 34:184–187
Monello RJ, Galloway NL, Powers JG, Madsen-Bouterse SA, Edwards WH, Wood ME, O'Rourke KI, Wild MA (2017) Pathogen-mediated selection in free-ranging elk populations infected by chronic wasting disease. P Natl Acad Sci USA 114:12208–12212. https://doi.org/10.1073/pnas.1707807114
Nishi JS, Shury T, Elkin BT (2006) Wildlife reservoirs for bovine tuberculosis (Mycobacterium bovis) in Canada: strategies for management and research. Vet Microbiol 112:325–338. https://doi.org/10.1016/j.vetmic.2005.11.013
Nunn CL, Jordan F, McCabe CM, Verdolin JF, Fewell JH (2015) Infectious disease and group size: more than just a numbers game. Philos Trans R Soc B 370:20140111. https://doi.org/10.1098/rstb.2014.0111
O’Brien PP, Webber QMR, Vander Wal E (2018) Consistent individual differences and population plasticity in network-derived sociality: an experimental manipulation of density in a gregarious ungulate. PLoS One 13:e0193425
Oraby T, Vasilyeva O, Krewski D, Lutscher F (2014) Modeling seasonal behavior changes and disease transmission with application to chronic wasting disease. J Theor Biol 340:50–59. https://doi.org/10.1016/j.jtbi.2013.09.003
Patterson JEH, Ruckstuhl KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology 140:803–813. https://doi.org/10.1017/S0031182012002259
Perkins SE, Cagnacci F, Stradiotto A, Arnoldi D, Hudson PJ (2009) Comparison of social networks derived from ecological data: Implications for inferring infectious disease dynamics. J Anim Ecol 78:1015–1022. https://doi.org/10.1111/j.1365-2656.2009.01557.x
Potapov A, Merrill E, Pybus M, Coltman D, Lewis MA (2013) Chronic wasting disease: possible transmission mechanisms in deer. Ecol Model 250:244–257. https://doi.org/10.1016/j.ecolmodel.2012.11.012
Proffitt KM, Gude JA, Hamlin KL, Garrott RA, Cunningham JA, Grigg JL (2011) Elk distribution and spatial overlap with livestock during the brucellosis transmission risk period. J Appl Ecol 48:471–478. https://doi.org/10.1111/j.1365-2664.2010.01928.x
Core Team R (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org
Ramos-Fernandez G, Boyer D, Gomez VP (2006) A complex social structure with fission – fusion properties can emerge from a simple foraging model. Behav Ecol Sociobiol 60:536–549. https://doi.org/10.1007/s00265-006-0197-x
Ruckstuhl KE (2007) Sexual segregation in vertebrates: proximate and ultimate causes. Integr Comp Biol 47:245–257. https://doi.org/10.1093/icb/icm030
Ruckstuhl KE, Neuhaus P (2000) Sexual segregation in ungulates: a new approach. Behaviour 137:361–377
Rushmore J, Caillaud D, Matamba L, Stumpf RM, Borgatti SP, Altizer S (2013) Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. J Anim Ecol 82:976–986. https://doi.org/10.1111/1365-2656.12088
Ryder JJ, Miller MR, White A, Knell RJ, Boots M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116:2017–2026. https://doi.org/10.1111/j.2007.0030-1299.15863.x
Schmid-Hempel P (2017) Parasites and their social hosts. Trends Parasitol 33:453–462. https://doi.org/10.1016/j.pt.2017.01.003
Shury TK, Bergeson D (2011) Lesion distribution and epidemiology of Mycobacterium bovis in elk and white-tailed deer in South-Western Manitoba, Canada. Vet Med Int 2011:591980–591911. https://doi.org/10.4061/2011/591980
Silk MJ, Drewe JA, Delahay RJ, Weber N (2018) Quantifying direct and indirect contacts for the potential transmission of infection between species using a multilayer contact network. Behaviour 155:731–757. https://doi.org/10.1163/1568539X-00003493
Smith MJ, Telfer S, Kallio ER, Kallio ER, Burthe S, Cook AR, Lambin X, Begon M (2009) Host-pathogen time series data in wildlife support a transmission function between density and frequency dependence. P Natl Acad Sci USA 106:7905–7909. https://doi.org/10.1073/pnas.0809145106
Tompkins DM, Dunn AM, Smith MJ, Telfer S (2011) Wildlife diseases: from individuals to ecosystems. J Anim Ecol 80:19–38. https://doi.org/10.1111/j.1365-2656.2010.01742.x
van Beest FM, McLoughlin PD, Vander Wal E, Brook RK (2014) Density-dependent habitat selection and partitioning between two sympatric ungulates. Oecologia 175:1155–1165. https://doi.org/10.1007/s00442-014-2978-7
Vander Wal E, Edye I, Paquet PC, Coltman DW, Bayne E, Brook RK, Andrés JA (2013a) Juxtaposition between host population structures: implications for disease transmission in a sympatric cervid community. Evol Appl 6:1001–1011. https://doi.org/10.1111/eva.12065
Vander Wal E, Laforge MP, McLoughlin PD (2014) Density dependence in social behaviour: home range overlap and density interacts to affect conspecific encounter rates in a gregarious ungulate. Behav Ecol Sociobiol 68:383–390. https://doi.org/10.1007/s00265-013-1652-0
Vander Wal E, Paquet PC, Andraés JA (2012a) Influence of landscape and social interactions on transmission of disease in a social cervid. Mol Ecol 21:1271–1282. https://doi.org/10.1111/j.1365-294X.2011.05431.x
Vander Wal E, Paquet PC, Messier F, Mcloughlin PD (2013b) Effects of phenology and sex on social proximity in a gregarious ungulate. Can J Zool 91:601–609. https://doi.org/10.1139/cjz-2012-0237
Vander Wal E, van Beest FM, Brook RK (2013c) Density-dependent effects on group size are sex-specific in a gregarious ungulate. PLoS One 8:e53777. https://doi.org/10.1371/journal.pone.0053777
Vander Wal E, Yip H, McLoughlin PD (2012b) Sex-based differences in density-dependent sociality: an experiment with a gregarious ungulate. Ecology 93:206–212. https://doi.org/10.1890/11-0020.1
VanderWaal KL, Obanda V, Omondi GP, McCowan B, Wang H, Fushing H, Isbell LA (2016) The “strength of weak ties” and helminth parasitism in giraffe social networks. Behav Ecol 27:1190–1197. https://doi.org/10.1093/beheco/arw035
Wasserberg G, Osnas EE, Rolley RE, Samuel MD (2009) Host culling as an adaptive management tool for chronic wasting disease in white-tailed deer: a modelling study. J Appl Ecol 46:457–466. https://doi.org/10.1111/j.1365-2664.2008.01576.x
Webber QMR, Czenze ZJ, Willis CKR (2015) Host demographic predicts ectoparasite dynamics for a colonial host during pre-hibernation mating. Parasitology 142:1260–1269. https://doi.org/10.1017/S0031182015000542
Webber QMR, Vander Wal E (2018) An evolutionary framework outlining the integration of individual social and spatial ecology. J Anim Ecol 87:113–127. https://doi.org/10.1111/1365-2656.12773
Weber N, Carter SP, Dall SRX, Delahay RJ, McDonald JL, Bearhop S, McDonald RA (2013) Badger social networks correlate with tuberculosis infection. Curr Biol 23:R915–R916. https://doi.org/10.1016/j.cub.2013.09.011
Weiss MN, Franks DW, Balcomb KC, Ellifrit DK, Silk MJ, Cant MA, Croft DP (2020) Modelling cetacean morbillivirus outbreaks in an endangered killer whale population. Biol Conserv 242:108398. https://doi.org/10.1016/j.biocon.2019.108398
Whitehead H, Dufault S (1999) Techniques for analyzing vertebrate social structure using identified individuals: review and recommendations. Adv Study Behav 28:33–74
Wilson ADM, Krause S, Ramnarine IW, Borner KK, Clément RJG, Kurvers RHJM, Krause J (2015) Social networks in changing environments. Behav Ecol Sociobiol 69:1617–1629. https://doi.org/10.1007/s00265-015-1973-2
Wolf JBW, Mawdsley D, Trillmich F, James R (2007) Social structure in a colonial mammal: unravelling hidden structural layers and their foundations by network analysis. Anim Behav 74:1293–1302. https://doi.org/10.1016/j.anbehav.2007.02.024
Acknowledgments
We respectfully acknowledge the RMNP data were collected within the traditional homeland of the Anishinabe people and the Métis Nation, within Treaty 2 territory and at the crossroads of Treaties 1 and 4. We thank Parks Canada Agency, Riding Mountain National Park, the University of Saskatchewan Western College of Veterinary Medicine Specialized Livestock Research Centre. We also thank T. Sallows, D. Bergeson, K. Kingdon, and T. Shury at Parks Canada as well as Phil Mcloughlin, Paul Paquet, and M. Woodbury. We thank A. Hurford, M. Laforge, M. Bonar, C. Hart, and S. Seissan-Zabihi as well as two anonymous reviewers for excellent comments on earlier versions of this manuscript.
Funding
This work was supported by a Natural Sciences and Engineering Research Council (NSERC, Canada) Doctoral Post-Graduate Scholarship (PGS-D) and Discovery Grant for EVW and a NSERC Vanier Canada Graduate Scholarship to QMRW.
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All applicable international, national, and/or institutional guidelines for the use of animals were followed. Statements of ethical approval, approval of research protocols, and capture procedures for both captive and free-ranging elk were approved by the University of Saskatchewan Animal Care Committee (Protocol number 20060067).
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Webber, Q.M.R., Vander Wal, E. Heterogeneity in social network connections is density-dependent: implications for disease dynamics in a gregarious ungulate. Behav Ecol Sociobiol 74, 77 (2020). https://doi.org/10.1007/s00265-020-02860-x
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DOI: https://doi.org/10.1007/s00265-020-02860-x