Do parasitism and nutritional status interact to affect production in snowshoe hares?

Ecology

Volumn 79, Issue 4, 1998, Pages 1209-1222

  Murray, Dennis L ^a,b   Keith, Lloyd B ^a   Cary, John R ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Body condition; Food supplementation; Interactive effects; Lepus americanus; Nutrition; Parasitism; Production; Snowshoe hare

Indexed keywords

BIOLOGICAL PRODUCTION; MAMMAL; NUTRITIONAL STATUS; PARASITISM;

ANIMALIA; DIROFILARIA; DIROFILARIA SCAPICEPS; LEPUS; LEPUS AMERICANUS; MAMMALIA; NEMATODA; NEMATODIRUS; NEMATODIRUS TRIANGULARIS; OBELISCOIDES; OBELISCOIDES CUNICULI; PROTOSTRONGYLUS; PROTOSTRONGYLUS BOUGHTONI; TRICHURIS; TRICHURIS LEPORIS; VERTEBRATA;

EID: 0031874978     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/0012-9658(1998)079[1209:DPANSI]2.0.CO;2     Document Type: Article

References (75)

1. Anderson, R. M., and D. M. Gordon. 1982. Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373-398.
2. Bailey, G. N. M. 1975. Energetics of a host-parasite system: a preliminary report. International Journal for Parasitology 5:609-613.
3. Bartlett, C. M. 1984. Development of Diroflaria scapiceps (Leidy, 1886) (Nematoda: Filarioidca) in lagomorphs. Canadian Journal of Zoology 62:965-979.
4. Bloomer, S. E. M., T. Willebrand, I. M. Keith, and L. B. Keith. 1995. Impact of helminth parasitism on a snowshoe hare population in central Wisconsin: A field experiment. Canadian Journal of Zoology 73:1891-1898.
5. Bookhout, T. A. 1971. Helminth parasites in snowshoe hares from northern Michigan. Journal of Wildlife Diseases 7: 246-248.
6. Boutin, S. 1984. Effect of late winter food addition on numbers and movements of snowshoe hares. Oecologia 62:393-400.
7. _. 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems and the future. Canadian Journal of Zoology 68:203-220.
8. Boutin, S., C. J. Krebs, R. Boonstra, M. R. T. Dale, S. J. Hannon, K. Martin, A. R. E. Sinclair, J. N. M. Smith, R. Turkington, M. Blower, A. Byrom, F. I. Doyle, C. Doyle, D. Hik, L. Hofer, A. Hubbs, T. Karels, D. L. Murray, V. Nams, M. O'Donoghue, C. Rohner, and S. Schweiger. 1995. Population changes of the vertebrate community during a snowshoe hare cycle in Canada's boreal forest. Oikos 74:69-80.
9. Boutin, S., C. J. Krebs, A. R. E. Sinclair, and J. N. M. Smith. 1986. Proximate causes of losses in a snowshoe hare population. Canadian Journal of Zoology 64:606-610.
10. Bryant, J. P. G. D. Wieland, T. Clausen, and P. Kuropat, 1985. Interactions of snowshoe hare and feltleaf willow in Alaska. Ecology 66:1564-1573.
11. Bundy, D. A. P. and M. H. N. Golden. 1987. The impact of host nutrition on gastrointestinal helminth populations. Parasitology 95:623-635.
12. Burkolder, W. J., and W. S. Swecker, 1990. Nutritional influences on immunity. Seminars in Veterinary Medicine and Surgery (Small Animal) 5:154-166.
13. Cary, J. R., and L. B. Keith. 1979. Reproductive change in the 10-year cycle of snowshoe hares. Canadian Journal of Zoology 57:375-390.
14. Connors, V. A., and B. B. NicKol. 1991. Effects of Plagiorhynchus cylindraceus (Acanthocephala) on the energy metabolism of adult starlings. Sturnus vulgaris. Parasitology 103:395-402.
15. Crawley, M. J. 1993. GLIM for Ecologists. Blackwell Scientific, Oxford, UK.
16. Crompton, D. W. T. 1991. Nutritional interactions between hosts and parasites. Pages 228-257 in C. A. Toft, A. Aeschlimann, and L. Bolis, editors. Parasite-host associations: coexistence or conflict? Oxford University Press, Oxford, UK.
17. Crompton, D. W. T., D. E. Walters, and S. Arnold. 1981. Changes in the food intake and body weight of protein-malnourished rats. Transactions of the Royal Society of Medicine and Hygiene 72:195-197.
18. Crompton, D. W. T., S. E. Arnold, D. E. Walters, and P. J. Whitfield. 1985. Food intake and body weight changes in mice infected with metacestodes of Taenia crussiceps. Parasitology 90:449-456.
19. Erickson, A. B. 1944. Helminth infections in relation to population fluctuations in snowshoc hares. Journal of Wildlife Management 8:134-153.
20. Forbes, M. R. L. 1993. Parasitism and host reproductive effort. Oikos 67:444-450.
21. Gulland, F. M. D. 1992. The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology 105:493-503.
22. Hall, A. 1985. Nutritional aspects of parasitic infection. Progress in Food and Nutrition Science 9:227-256.
23. Hanks, J. 1981. Characterization of population condition. Pages 47-73 in C. W. Fowler and T. D. Smith, editors. Dynamics of large mammal populations. John Wiley and Sons, New York, New York, USA.
24. Holmes, J. C. 1995. Population regulation: a dynamic complex of interactions. Wildlife Research 22:11-20.
25. Holmes, J. C., and P. W. Price. 1986. Communities of parasites. Pages 187-213 in J. Kikkawa and D. J. Anderson. editors. Community ecology: pattern and process. Blackwell Scientific, London, UK.
26. Hosmer, D. W., and S. Lemeshow. 1989. Applied logistic regression. John Wiley and Sons, New York, New York, USA.
27. Hudson, P. J. 1986. The effect of a parasitic nematode on the breeding production of red grouse. Journal of Animal Ecology 55:85-92.
28. Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187-211.
29. Jogia, M. K., A. R. H. Sinclair, and R. J. Andersen. 1989. An antifeedant in balsam poplar inhibits browsing by snowshoe hares. Oecologia 79:189-192.
30. Karasov, W. H. 1986. Energetics, physiology and vertebrate ecology. Trends in Ecology and Evolution 1:101-104.
31. Keith, I. M., L. B. Keith, and J. R. Cary. 1986. Parasitism in a declining population of snowshoe hares. Journal of Wildlife Diseases 22:349-363.
32. Keith, L. B. 1990. Dynamics of snowshoe hare populations. Pages 1 19-195 in H. H. Genoways, editor. Current Mammalogy. Plenum Press, New York, New York, USA.
33. Keith, L. B., and D. H. Rusch. 1988. Predation's role in the cyclic fluctuations of ruffed arouse. Acta XIX Congress of International Ornithologists 19:699-732.
34. Keith, L. B., E. C. Meslow, and O. J. Rongstad. 1968. Techniques for snowshoe hare population studies. Journal of Wildlife Management 32:801-812.
35. Keith, L. B., J. R. Cary, O. J. Rongstad, and M. C. Brittingham. 1984. Demography and ecology of a declining snowshoe hare population. Wildlife Monographs 90.
36. Keith, L. B., J. R. Cary, T. M. Yuill, and I. M. Keith. 1985. Prevalence of helminths in a cyclic snowshoe hare population. Journal of Wildlife Diseases 21:233-253.
37. Keymer, A. E., and A. P. Dobson. 1987. The ecology of helminths in populations of small mammals. Mammal Reviews 17:105-116.
38. Keymer, A., D. W. T. Crompton. and D. E. Walters. 1983. Nippostrongylus (Nematoda) in protein-malnourished rats: host mortality, morbidity and rehabilitation. Parasitology 86:461-475.
39. Korpimäki, E., H. Hakkarainen, and G. F. Bennett. 1993. Blood parasites and reproductive success of Tengmalm's owls: detrimental effects on females but not on males? Functional Ecology 7:420-426.
40. Kralka, R. A., and W. M. Samuel. 1984. Experimental life cycle of Protostrongylus boutghtoni (Nematoda: Metastrongyloidea), a lung worm of snow shoe hares, Lepus americanus. Canadian Journal of Zoology 62:473-479.
41. Krebs, C. J. 1989. Ecological Methodology. Harper and Row, New York, New York, USA.
42. Krebs, C. J., S. Boutin, and B. S. Gilbert. 1986a. A natural feeding experiment on a declining snowshoe hare population. Oecologia 70:194-197.
43. Krebs, C. J., B. S. Gilbert, S. Boutin, A. R. E. Sinclair, and J. N. M. Smith. 1986b. Population biology of snowshoe hares. I. Demography of food-supplemented populations in the southern Yukon, 1976-84. Journal of Animal Ecology 55:963-982.
44. Laine, K., and H. Henttonen. 1983. The role of plant production in microtine cycles in northern Fennoscandinavia. Oikos 40:407-418.
45. Margolis, L., G. W. Esch, J. C. Holmes, A. M. Kuris, and G. M. Schad. 1982. The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68:131-133.
46. Measures, L. N., and R. C. Anderson. 1983. Characteristics of natural infections of the stomachworm. Obeliscoides cuniculi (Graybill), in lagomorphs and woodchucks in Canada. Journal of Wildlife Diseases 19:219-224.
47. Mihook, S., B. N. Turner, and S. L. Iverson. 1985. The characterization of vole population dynamics. Ecological Monographs 55:399-420.
48. Minchella, D. J., and M. E. Scott. 1991. Parasitism: a cryptic determinant of animal community structure. Trends in Ecology and Evolution 6:250-254.
49. Moller, A. P. 1993. Ectoparasites increase the cost of reproduction in their hosts. Journal of Animal Ecology 62:309-322.
50. Moller, A. P. 1994. Parasites as an environmental component of reproduction in birds. Ardea 82:161-172.
51. Møller, A. P., F. de Lope, J. Moreno, G. GonZàlez, and J. J. Pérez. 1994. Ectoparasites and host energetics: house martin bugs and house martin nestlings. Oecologia 98:263-268.
52. Mutiger, J. C., and W. H. Karasov. 1989. Sublethal parasites and host energy bugets: tapeworm infection in white-footed mice. Ecology 70:904-921.
53. Munger, J. C., and W. H. Karasov. 1991. Sublethal parasites in white-footed mice: impact on survival and reproduction. Canadian Journal of Zoology. 69:398-404.
54. Munger, J. C., and W. H. Karasov. 1994. Costs of bot fly infection in white-footed mice: energy and mass flow. Canadian Journal of Zoology 72:166-173.
55. Murray, D. L., L. B. Keith, and J. R. Cary. 1996. The efficacy of anthelminthic treatment on the parasite abundance of free-ranging snowshoe hares. Canadian Journal of Zoology 74:1604-1611.
56. Murray, D. L., J. R. Cary, and L. B. Keith. 1997. Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology 66:250-264.
57. Neter, J., W. Wasserman, and M. H. Kunter. 1990. Applied linear statistical models. Irwin, Homewood, Illinois. USA.
58. O'Donoghue, M., and C. J. Krebs. 1992. Effects of supplemental food on snowshoe hare reproduction and juvenile growth at a cyclic population peak. Journal of Animal Ecology 61:631-641.
59. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223-225.
60. Richner, H., A. Oppliger, and P. Christe. 1993. Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology 62:703-710.
61. Robbins, C. T. 1993. Wildlife feeding and nutrition. Academic Press, San Diego, California, USA.
62. Rusch, D. H., M. M. Gillespie, and D. E. McKay. 1978. Decline of a ruffed grouse population in Manitoba. Canadian Field-Naturalist 92:123-127.
63. Schall, J. J., A. F. Bennett, and R. W. Pulnam. 1982. Lizards infected with malaria: physiological and behavioral consequences. Science 217:1057-1059.
64. Scott, M. E. 1988. The impact of infection and disease on animal populations: implications for conservation biology. Conservation Biology 2:40-56.
65. Sinclair, A. R. E., and J. N. M. Smith. 1984. Do plant secondary compounds determine feeding preferences of snowshoe hares? Oecologia 61:403-410.
66. Slater, A. F. G., and A. E. Keymer. 1986. Heligmosomoides polygyrus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proceedings of the Royal Society of London Series B 229:69-83.
67. Smith, J. N. M., C. J. Krebs, A. R. E. Sinclair, and R. Boonstra. 1988. Population biology of snowshoe hares. II. Interactions with winter food plants. Journal of Animal Ecology 57:269-286.
68. Solomons, N. W., and M. E. Scott. 1994. Nutritional status of host populations influences parasitic infections. Pages 101-114 in M. E. Scott and G. Smith, editors. Parasitic and infectious diseases. Academic Press, New York, New York, USA.
69. Steel, R. D. G., and J. H. Torrie. 1980. Principles and procedures of statistics. McGraw-Hill, New York, New York, USA.
70. Toque, K. 1993. The relationship between parasite burden and host resources in the desert toad (Scaphiopus couchii), under natural conditions. Journal of Animal Ecology 62: 683-693.
71. Tripet, E. and H. Richner. 1997. Host responses to ectoparasites: food compensation by parent blue tits. Oikos 78: 557-561.
72. Wakelin, D. 1987. The role of the immune response in helminth population regulation. International Journal for Parasitology 17:291-297.
73. Warren, R. J., and R. L. Kirkpatrick. 1978. Indices of nutritional status in cottontail rabbits fed controlled diets. Journal of Wildlife Management 42:154-158.
74. Wolff, J. O. 1980. The role of habitat patchiness in the population dynamics of snowshoe hares. Ecological Monographs 50:111-130.
75. Yuill, T. M. 1987. Diseases as components of mammalian ecosystems: mayhem and subtlety. Canadian Journal of Zoology 65:1061-1066.