Immunochallenge reduces risk sensitivity during foraging in white-footed mice

Animal Behaviour

Volumn 83, Issue 1, 2012, Pages 155-161

  Schwanz, Lisa E ^a   Previtali, M Andrea ^a   Gomes Solecki, Maria ^b   Brisson, Dustin ^c   Ostfeld, Richard S ^a  

^a CARY INSTITUTE OF ECOSYSTEM STUDIES   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Behaviourally mediated trophic cascade; Ecology of fear; Giving up density; Peromyscus leucopus; Quitting harvest rate; Trait mediated indirect effect; White footed mouse

Indexed keywords

DISEASE VECTOR; FITNESS; FOOD PREFERENCE; FORAGING BEHAVIOR; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; LIFE HISTORY TRAIT; MORTALITY; PARASITIC DISEASE; PATCHINESS; RODENT; TICK; TROPHIC CASCADE;

UNITED STATES;

IXODIDA; MUS; PEROMYSCUS; PEROMYSCUS LEUCOPUS;

EID: 83555165912     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2011.10.020     Document Type: Article

References (75)

1. Abrams P.A. Foraging time optimization and interactions in food webs. American Naturalist 1984, 124:80-96.
2. Adamo S.A. Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Animal Behaviour 1999, 57:117-124.
3. Beckerman A.P., Uriarte M., Schmitz O.J. Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. Proceedings of the National Academy of Sciences, U.S.A. 1997, 94:10735-10738.
4. Bertrand S., Criscuolo F., Faivre B., Sorci G. Immune activation increases susceptibility to oxidative tissue damage in zebra finches. Functional Ecology 2006, 20:1022-1027.
5. Biro P.A., Dingemanse N.J. Sampling bias resulting from animal personality. Trends in Ecology & Evolution 2008, 24:66-67.
6. Brown J.S. Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology 1988, 22:37-47.
7. Brown J.S. Patch use under predation risk: I. Models and predictions. Annales Zoologici Fennici 1992, 29:301-309.
8. Brown J.S., Kotler B.P. Hazardous duty pay and the foraging cost of predation. Ecology Letters 2004, 7:999-1014.
9. Brown J.S., Kotler B.P. Foraging and the ecology of fear. Foraging: Behavior and Ecology 2007, 437-480. University of Chicago Press, Chicago. D.W. Stephens, J.S. Brown, R.C. Ydenberg (Eds.).
10. Brunner J.L., LoGiudice K., Ostfeld R.S. Estimating the importance of zoonotic reservoir hosts in pathogen transmission: prevalence and infectivity, sensitivity and specificity. Journal of Medical Entomology 2008, 45:139-147.
11. Bunikis J., Tsao J., Luke C.J., Luna M.G., Fish D., Barbour A.G. Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: a longitudinal study in an area where Lyme borreliosis is highly endemic. Journal of Infectious Diseases 2004, 189:1515-1523.
12. Burgdorfer W., Barbour A.G., Hayes S.F., Benach J.L., Grunwaldt E., Davis J.P. Lyme disease: a tick-borne spirochetosis?. Science 1982, 216:1317-1319.
13. Burns C.E., Goodwin B.J., Ostfeld R.S. A prescription for longer life? Bot fly parasitism of the white-footed mouse. Ecology 2005, 86:753-761.
14. Canty A., Ripley B. Boot: Bootstrap R (S-plus) Functions. R Package, Version 1.2-41 2009, http://cran.r-project.org/web/packages/boot/.
15. Charnov E.L. Optimal foraging, the marginal value theorem. Theoretical Population Biology 1976, 9:129-136.
16. Clark C.W. Antipredator behavior and the asset-protection principle. Behavioral Ecology 1994, 5:159-170.
17. Connors M.J., Schauber E.M., Forbes A., Jones C.G., Goodwin B.J., Ostfeld R.S. Use of track plates to quantify predation risk at small spatial scales. Journal of Mammalogy 2005, 86:991-996.
18. Deavers D.R., Hudson J.W. Water metabolizing in two small rodents and an insectivore. Physiological Zoology 1979, 52:137-152.
19. Demas G.E. The energetic of immunity: a neuroendocrine link between energy balance and immune function. Hormones and Behavior 2004, 45:173-180.
20. Derting T.L., Compton S. Immune response, not immune maintenance, is energetically costly in wild white-footed mice (Peromyscus leucopus). Physiological and Biochemical Zoology 2003, 76:744-752.
21. Fikrig E., Barthold S.W., Kantor F.S., Flavell R.A. Protection of mice against the Lyme disease agent by immunizing with a recombinant OspA. Science 1990, 250:553-556.
22. Fokidis H.B., Robertson C., Risch T.S. Keeping tabs: are redundant marking systems needed for rodents?. Wildlife Society Bulletin 2006, 34:764-771.
23. Gibbons J.W., Andrews K.M. PIT tagging: simple technology at its best. BioSciences 2004, 54:447-454.
24. Gilliam J.F., Fraser D.F. Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 1987, 68:1856-1862.
25. Godin J.-G.J., Smith S.A. A fitness cost of foraging in the guppy. Nature 1988, 333:69-71.
26. Godin J.-G.J., Sproul C.D. Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability. Canadian Journal of Zoology 1988, 66:2360-2367.
27. Gomes-Solecki M.J.C., Brisson D.R., Dattwyler R.J. Oral vaccine that breaks the transmission cycle of the Lyme disease spirochete can be delivered via bait. Vaccine 2006, 24:4440-4449.
28. Hill R.W. The amount of maternal care in Peromyscus leucopus and its thermal significance for the young. Journal of Mammalogy 1972, 53:774-790.
29. Hill R.W. Thermal physiology and energetics of Peromyscus: ontogeny, body temperature, metabolism, insulation, and microclimatology. Journal of Mammalogy 1983, 64:19-37.
30. Holmes J.C., Zohar S. Pathology and host behaviour. Parasitism and Host Behavior 1990, 34-63. Taylor & Francis, New York. C.J. Barnard, J.M. Behnke (Eds.).
31. Hofmeister E.K., Ellis B.A., Glass G.E., Childs J.E. Longitudinal study of infection with Borrelia burdorferi in a population of Peromyscus leucopus at a Lyme disease-enzootic site in Maryland. American Journal of Tropical Medicine and Hygiene 1999, 60:598-609.
32. Jones C.G., Ostfeld R.S., Richard M.P., Schauber E.M., Wolff J.O. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 1998, 279:1023-1026.
33. Kauffman M.J., Brodie J.F., Jules E.S. Are wolves saving Yellowstone's aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology 2010, 91:2742-2755.
34. Keesing F., Brunner J., Duerr S., Killilea M., LoGiudice K., Schmidt K., Vuong H., Ostfeld R.S. Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society B 2009, 276:3911-3919.
35. Klasing K.C. The costs of immunity. Acta Zoologica Sinica 2004, 50:961-969.
36. Kotler B.P. Patch use by gerbils in a risky environment: manipulating food and safety to test four models. Oikos 1997, 78:274-282.
37. Kotler B.P., Brown J.S. Community ecology. Foraging: Behavior and Ecology 2007, 397-434. University of Chicago Press, Chicago. D.W. Stephens, J.S. Brown, R.C. Ydenberg (Eds.).
38. Kotler B.P., Brown J.S., Bouskila A. Apprehension and time allocation in gerbils: the effects of predatory risk and energetic state. Ecology 2004, 85:917-922.
39. Laundré J.W., Hernández L., Altendorf K.B. Wolves, elk, bison: reestablishing the 'landscape of fear' in Yellowstone National Park, USA. Canadian Journal of Zoology 2001, 79:1401-1409.
40. Levine J.F., Wilson M.L., Spielman A. Mice as reservoirs of the Lyme disease spirochete. American Journal of Tropical Medicine and Hygiene 1985, 34:355-360.
41. Lima S.L. Initiation and termination of daily feeding in dark-eyed juncos: influences of predation risk and energy reserves. Oikos 1988, 53:3-11.
42. Lima S.L., Dill L.M. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 1990, 68:619-640.
43. Lochmiller R.L., Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity?. Oikos 2000, 88:87-98.
44. LoGiudice K., Ostfeld R.S., Schmidt K.A., Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, U.S.A. 2003, 100:567-571.
45. Luke C.J., Heubner R.C., Kasmiersky V., Barbour A.G. Oral delivery of purified lipoprotein OspA protects mice from systemic infection with Borrelia burgdorferi. Vaccine 1997, 15:739-746.
46. McNamara J.M., Houston A.I. The common currency for behavioral decisions. American Naturalist 1986, 127:358-378.
47. Martin L.B., Weil Z.M., Kuhlman J.R., Nelson R.J. Trade-offs within the immune systems of female white-footed mice, Peromyscus leucopus. Functional Ecology 2006, 20:630-636.
48. Milinski M. Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 1985, 93:203-216.
49. Morris D.W., Davidson D.L. Optimally foraging mice match patch use with habitat differences in fitness. Ecology 2000, 81:2061-2066.
50. Munger J.C., Karasov W.H. Sublethal parasites in white-footed mice: impact on survival and reproduction. Canadian Journal of Zoology 1991, 69:398-404.
51. Munger J.C., Karasov W.H. Costs of bot fly infection in white-footed mice: energy and mass flow. Canadian Journal of Zoology 1994, 72:166-173.
52. Nilsson J.- Å, Granbom M., Råberg L. Does the strength of an immune response reflect its energetic cost?. Journal of Avian Biology 2007, 38:488-494.
53. Ostfeld R.S., Jones C.G., Wolff J.O. Of mice and mast. Bioscience 1996, 46:323-330.
54. Ostfeld R.S., Hazler K.R., Cepeda O.M. Temporal and spatial dynamics of Ixodes scapularis (Acari: Ixodidae) in a rural landscape. Journal of Medical Entomology 1996, 33:90-95.
55. Ostfeld R.S., Miller M.C., Hazler K.R. Causes and consequences of tick (Ixodes scapularis) burdens on white-footed mice (Peromyscus leucopus). Journal of Mammalogy 1996, 77:266-273.
56. Poulin R. Age-dependent effects of parasites on anti-predator responses in two New Zealand freshwater fish. Oecologia 1993, 96:431-438.
57. Poulin R. Meta-analysis of parasite-induced behavioural changes. Animal Behaviour 1994, 48:137-146.
58. R Development Core Team 2009. R: a Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
59. Raveh A., Kotler B.P., Abramsky Z., Krasnov B.R. Driven to distraction: detecting the hidden costs of flea parasitism through foraging behavior in gerbils. Ecology Letters 2011, 14:47-51.
60. Ripple W.J., Beschta R.L. Restoring Yellowstone's aspen with wolves. Biological Conservation 2007, 138:514-519.
61. Ripple W.J., Larsen E.J., Renkin R.A., Smith D.W. Trophic cascades among wolves, elk and aspen on Yellowstone National Park's northern range. Biological Conservation 2001, 102:227-234.
62. Schmidt K.A., Ostfeld R.S. Songbird populations in fluctuating environments: predator responses to pulsed resources. Ecology 2003, 84:406-415.
63. Schmidt K.A., Ostfeld R.S. Mice in space: space use predicts the interaction between mice and songbirds. Ecology 2003, 84:3276-3283.
64. Schmidt K.A., Schauber E.M. Behavioral indicators of predator space use: studying species interactions through the behavior of predators. Israel Journal of Ecology and Evolution 2007, 53:389-406.
65. Schmidt K.A., Goheen J.R., Naumann R. Incidental nest predation in songbirds: behavioral indicators detect ecological scale and processes. Ecology 2001, 82:2937-2947.
66. Schwanz L.E., Brisson D., Gomes-Solecki M., Ostfeld R.S. Linking disease and community ecology through behavioural indicators: immunochallenge of white-footed mice and its ecological impacts. Journal of Animal Ecology 2011, 80:204-214.
67. Schwanz L.E., Voordouw M.J., Brisson D., Ostfeld R.S. Borrelia burgdorferi has minimal impact on the Lyme disease reservoir host Peromyscus leucopus. Vector-borne and Zoonotic Diseases 2011, 11:117-124.
68. Sikes R.S., Gannon W.L., the Animal Care and Use Committee of the American Society of Mammalogists Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 2011, 92:235-253.
69. de Silva A.M., Telford S.R., Brunet L.R., Barthold S.W., Fikrig E. Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine. Journal of Experimental Medicine 1996, 183:271-275.
70. Thomas F., Poulin R., de Meeüs T., Guégan J.-F., Renaud F. Parasites and ecosystem engineering: what roles could they play?. Oikos 1999, 84:167-171.
71. Tompkins D.M., Dunn A.M., Smith M.J., Telfer S. Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 2011, 80:19-38.
72. Velando A., Drummond H., Torres R. Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proceedings of the Royal Society B 2006, 273:1443-1448.
73. Weil Z.M., Martin L.B., Workman J.L., Nelson R.J. Immune challenge retards seasonal reproductive regression in rodents: evidence for terminal investment. Biology Letters 2006, 2:393-396.
74. Wood C.L., Byers J.E., Cottingham K.L., Altman I., Donahue M.J., Blakeslee M.H. Parasites alter community structure. Proceedings of the National Academy of Sciences, U.S.A. 2007, 104:9335-9339.
75. Zuk M., Stoehr A.M. Immune defense and host life history. American Naturalist 2002, 160:S9-S22.