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Ecological determinants of pathogen transmission in communally roosting species

  • Andrew J. LaughlinEmail author
  • Richard J. Hall
  • Caz M. Taylor
ORIGINAL PAPER

Abstract

Many animals derive benefits from roosting communally but may also face increased risk of infectious disease transmission. In spite of recent high-profile disease outbreaks in roosting animals of conservation and public health concern, we currently lack general theory for how attributes of roosting animals and their pathogens influence pathogen spread among roosts and overall population impacts on roosting species. Here we develop a model to explore how roost size and host site fidelity influence the time for a pathogen to escape from its initial roost, overall infection prevalence, and host population size, for pathogens with density- or frequency-dependent transmission and varying virulence. We find that pathogens spread rapidly to all roosts when animals are distributed among a small number of large roosts, and that roost size more strongly influences spread rate for density-dependent than frequency-dependent transmitted pathogens. However, roosting animals that exhibit high site fidelity and distribute among a large number of small roosts are buffered from population-level impacts of pathogens of both transmission modes. We discuss our results in the context of anthropogenic change that is altering aspects of roosting behavior relevant to emerging pathogen spread.

Keywords

Animal aggregations Communal roost Pathogen transmission Roost size Site fidelity 

Notes

Acknowledgements

We wish to thank the three anonymous reviewers whose suggestions helped improve the clarity of the manuscript.

Funding information

This material is based upon work supported by the National Science Foundation under grant no. DEB-1754392 (CMT, RJH) and DEB-1518611(RJH), a Tulane University Department of Ecology and Evolutionary Biology one-term Dissertation Fellowship (AJL) and by a scholar award from the James S. McDonnell Foundation (CMT).

References

  1. Allen G (1984) The effect of disturbance on harbor seal haul out patterns at Bolinas Lagoon, California. Fish Bull 82:493–500Google Scholar
  2. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467–484CrossRefGoogle Scholar
  3. Arino J, Davis JR, Hartley D, Jordan R, Miller JM, Van Den Driessche P (2005) A multi-species epidemic model with spatial dynamics. Math Med Biol 22(2):129–142CrossRefGoogle Scholar
  4. Beauchamp G (1999) The evolution of communal roosting in birds: origin and secondary losses. Behav Ecol 10:675–687CrossRefGoogle Scholar
  5. Becker DJ, Hall RJ (2016) Heterogeneity in patch quality buffers metapopulations from pathogen impacts. Theor Ecol 9(2):197–205CrossRefGoogle Scholar
  6. Bradley CA, Altizer S (2005) Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecol Lett 8(3):290–300CrossRefGoogle Scholar
  7. Cleveland CJ, Betke M, Federico P, Frank JD, Hallam TG, Horn J, López JD, McCracken GF, Medellín RA, Moreno-Valdez A, Sansone CG, Westbrook JK, Kunz TH (2006) Economic value of the pest control service provided by Brazilian free-tailed bats in south-central Texas. Front Ecol Environ 4(5):238–243Google Scholar
  8. Clough S, Ladle M (1997) Diel migration and site fidelity in a stream-dwelling cyprinid, Leuciscus leuciscus. J Fish Biol 50:1117–1119Google Scholar
  9. Daoud-Opit S, Jones DN (2016) Guided by the light: roost choice and behaviour of urban rainbow lorikeets (Trichoglossus haematodus). Eur J Ecol 2(1):72–80CrossRefGoogle Scholar
  10. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287(5452):443–449CrossRefGoogle Scholar
  11. Dawson JR, Stone WB, Ebel GD, Young DS, Galinski DS et al (2007) Crow deaths caused by West Nile virus during winter. Emerg Infect Dis 13:1912–1914CrossRefGoogle Scholar
  12. Deka MA, Morshed N (2018) Mapping disease transmission risk of nipah virus in south and Southeast Asia. Trop Med Infect Dis 3(2):1Google Scholar
  13. Diuk-Wasser MA, Molaei G, Simpson JE, Folsom-O’Keefe CM, Armstrong PM, Andreadis TM (2010) Avian communal roosts as amplification foci for West Nile virus in urban areas in northeastern United States. Am J Trop Med Hyg 82:337–343CrossRefGoogle Scholar
  14. Duchamp JE, Sparks DW, Swihart RK (2010) Exploring the “nutrient hot spot” hypothesis at trees used by bats. J Mammal 91(1):48–53Google Scholar
  15. Eiserer LA (1984) Communal roosting in birds. Bird Behav 5:61–80Google Scholar
  16. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329:679–682CrossRefGoogle Scholar
  17. Grether GF, Switzer PV (2000) Mechanisms for the formation and maintenance of traditional night roost aggregations in a territorial damselfly. Anim Behav 60:569–579CrossRefGoogle Scholar
  18. Grether GF, Aller TL, Grucky NK, Levi A, Antaky CC, Townsend VR Jr (2014) Species differences and geographic variation in the communal roosting behavior of Prionostemma harvestmen in Central American rainforests. J Arachnol 42:257–267CrossRefGoogle Scholar
  19. Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311CrossRefGoogle Scholar
  20. Hamilton WJ (1982) Baboon sleeping site preferences and relationships to primate grouping patterns. Amer J Primat 3:41–53CrossRefGoogle Scholar
  21. Hawley DM, Davis AK, Dhondt AA (2007) Transmission-relevant behaviours shift with pathogen infection in wild house finches (Carpodacus mexicanus). Can J Zool 85(6):752–757CrossRefGoogle Scholar
  22. Janousek WM, Marra PP, Kilpatrick AM (2014) Avian roosting behavior influences vector-host interactions for West Nile virus hosts. Parasite Vector 7(1):399CrossRefGoogle Scholar
  23. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  24. Kunz TH (1982) Roosting ecology of bats. In: Kunz TH (ed) Ecology of bats. Springer, New York, pp 1–55CrossRefGoogle Scholar
  25. Langwig KE, Frick WF, Bried JT, Hicks AC, Kunz TH, Kilpatrick AM (2012) Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol Lett 15(9):1050–1057CrossRefGoogle Scholar
  26. Langwig KE, Frick WF, Reynolds R, Parise KL et al (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc R Soc Lond B Biol Sci 282:20142335CrossRefGoogle Scholar
  27. Laughlin AJ, Sheldon DR, Winkler DW, Taylor CM (2014) Behavioral drivers of communal roosting in a songbird: a combined theoretical and empirical approach. Behav Ecol 25:734–743CrossRefGoogle Scholar
  28. Leyrer J, Spaans B, Camara M, Piersma T (2006) Small home ranges and high site fidelity in red knots (Calidris canuts canutus) wintering on the Banc d’Arguin, Mauritania. J Ornith 147:376–384CrossRefGoogle Scholar
  29. Lilleyman A, Franklin DC, Szabo JK, Lawes MJ (2016) Behavioural responses of migratory shorebirds to disturbance at a high-tide roost. Emu-Austral Ornithol 116(2):111–118CrossRefGoogle Scholar
  30. Lorch JM, Muller LK, Russell RE, O’Connor M, Lindner DL et al (2013) Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. Appl Environ Microbiol 79:1293–1301CrossRefGoogle Scholar
  31. Maher SP, Kramer AM, Pulliam JT, Zokan MA, Bowden SE, Barton HD, Magori K, Drake JM (2012) Spread of white-nose syndrome on a network regulated by geography and climate. Nat Commun 3:1306CrossRefGoogle Scholar
  32. Mallet J (1986) Gregarious roosting and home range in Heliconius butterflies. Natl Geogr Res 2:198–215Google Scholar
  33. McCormack RK, Allen LJ (2007) Multi-patch deterministic and stochastic models for wildlife diseases. J Biol Dyn 1(1):63–85CrossRefGoogle Scholar
  34. Neubaum DJ, Wilson KR, O'Shea TJ (2007) Urban maternity-roost selection by big brown bats in Colorado. J Wildl Manag 71(3):728–736CrossRefGoogle Scholar
  35. O’Donnell CFJ, Sedgeley JA (1999) Use of roosts by the long-tailed bat, Chalinolobus tuberculatus, in temperate rainforest in New Zeal. J Mammal 80:813–923Google Scholar
  36. O'Shea TJ, Bogan MA (2003) Monitoring trends in bat populations of the United States and territories: problems and prospects. Biological Resources Discipline, Information and Technology Report USGS/BRD/ITR-2003-003. U.S. Geological Survey, Washington, DCGoogle Scholar
  37. Parrish JK, Edelstein-Keshet L (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284:99–101CrossRefGoogle Scholar
  38. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, Daszak P (2011) Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc R Soc B 278(1725):3703–3712CrossRefGoogle Scholar
  39. Ryder JJ, Miller MR, White A, Knell RJ, Boots M (2007) Host-parasite population dynamics under combined frequency-and density-dependent transmission. Oikos 116:2017–2026CrossRefGoogle Scholar
  40. Streicker DG, Recuenco S, Valderrama W, Gomez Benavides J, Vargas I, Pacheco V, Condori Condori RE et al (2012) Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control. Proc R Soc B 279:3384–3392CrossRefGoogle Scholar
  41. Swinton J, Harwood J, Grenfell BT, Gilligan CA (1998) Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations. J Anim Ecol 67:54–68CrossRefGoogle Scholar
  42. Thompson PM (1989) Seasonal changes in the distribution and composition of common seal (Phoca vitulina) haul-out groups. J Zool 217:281–294CrossRefGoogle Scholar
  43. Ward P, Zahavi A (1973) The importance of certain assemblages of birds as “information-centres” for food-finding. Ibis 115:517–534CrossRefGoogle Scholar
  44. Yadon VL (1956) The artificial roost: an aid in population studies. J Wildl Manag 20:466CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Andrew J. Laughlin
    • 1
    Email author
  • Richard J. Hall
    • 2
    • 3
    • 4
  • Caz M. Taylor
    • 5
  1. 1.Department of Environmental StudiesUniversity of North Carolina at AshevilleAshevilleUSA
  2. 2.Odum School of EcologyUniversity of GeorgiaAthensUSA
  3. 3.Department of Infectious Diseases, College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  4. 4.Center for the Ecology of Infectious DiseasesUniversity of GeorgiaAthensUSA
  5. 5.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA

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