Innate immunity in free-ranging African buffalo (Syncerus caffer): Associations with parasite infection and white blood cell counts

Physiological and Biochemical Zoology

Volumn 85, Issue 3, 2012, Pages 255-264

  Beechler, Brianna R ^a   Broughton, Heather ^a   Bell, Austin ^a   Ezenwa, Vanessa O ^b,c   Jolles, Anna E ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; BODY CONDITION; CATTLE; CORRELATION; IMMUNE RESPONSE; IMMUNITY; LIFE HISTORY TRAIT; PARASITE INFESTATION; SPATIOTEMPORAL ANALYSIS;

ANIMAL; ANIMAL DISEASE; ARTICLE; BLOOD; BLOOD ANALYSIS; BUFFALO; COCCIDIA; COCCIDIOSIS; EVALUATION; FECES; FEMALE; GASTROINTESTINAL TRACT; IMMUNOLOGY; INNATE IMMUNITY; LEUKOCYTE COUNT; METHODOLOGY; MICROBIOLOGY; MYCOBACTERIUM BOVIS; NEMATODE; NEMATODIASIS; PARASITE IDENTIFICATION; PARASITOLOGY; PHYSIOLOGY; SEASON; SERUM BACTERICIDAL ACTIVITY; SOUTH AFRICA; TICK; TICK INFESTATION; TUBERCULOSIS;

ANIMALS; BLOOD BACTERICIDAL ACTIVITY; BLOOD CHEMICAL ANALYSIS; BUFFALOES; COCCIDIA; COCCIDIOSIS; FECES; FEMALE; GASTROINTESTINAL TRACT; IMMUNITY, INNATE; LEUKOCYTE COUNT; MYCOBACTERIUM BOVIS; NEMATODA; NEMATODE INFECTIONS; PARASITE EGG COUNT; SEASONS; SOUTH AFRICA; TICK INFESTATIONS; TICKS; TUBERCULOSIS;

KRUGER NATIONAL PARK; SOUTH AFRICA;

ANIMALIA; BOVIDAE; BOVINAE; COCCIDIA; IXODIDA; MAMMALIA; NEMATODA; SYNCERUS CAFFER;

EID: 84859736702     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/665276     Document Type: Article

References (65)

1. Abbas A.K., K.M. Murphy, and A. Sher. 1996. Functional diversity of helper T-lymphocytes. Nature 383:787-793.
2. Allen L.C., A.S. Turmelle, M.T. Mendonca, K.J. Navara, T.H. Kunz, and G.F. McCracken. 2009. Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (Tadarida brasiliensis). J Comp Physiol B 179:315-323.
3. Alonso-Alvarez C. and J.L. Tella. 2001. Effects of experimental food restriction and body-mass changes on the avian T-cell mediated immune response. Can J Zool 79:101-105.
4. Aly K., S. Darwish, A. Ramoun, K. Tawfeek, N. Hanh, N. Sousa, J. Sulon, O. Szenci, and J.F. Beckers. 2011. Accuracy of transrectal palpation for early pregnancy diagnosis in Egyptian buffaloes. Trop Anim Health Prod 43:5-7.
5. Ardia D.R., H.K. Parmentier, and L.A. Vogel. 2011. The role of constraints and limitation in driving individual variation in immune response. Funct Ecol 25:61-73.
6. Bengis R., R. Grant, and V. deVos. 2003. Wildlife diseases and veterinary controls: a savanna ecosystem perspective. Pp. 349-369 in H.C. Biggs, J.T. du Toit, K. Johan, K. Rogers, A. Sinclair, and B. Walker, eds. The Kruger experience: ecology and management of savannah heterogeneity. Island, Washington, DC.
7. Betelli E., M. Oukka, and V.K. Kuchroo. 2007. TH-17 cells in the circle of immunity and autoimmunity. Nat Rev Immunol 8:345-350.
8. Boughton R.K., G. Joop, and S.A.O. Armitage. 2011. Outdoor immunology: methodological considerations for ecologists. Funct Ecol 25:81-100.
9. Bradley J.E. and J.A. Jackson. 2008. Measuring immune system variation to help understand host-pathogen community dynamics. Parasitology 135:807-823.
10. Buehler D.M., T. Piersma, K. Matson, and B.I. Tieleman. 2008. Seasonal redistribution of immune function in a migrant shorebird: annual cycle effects override adjustments to thermal regime. Am Nat 172:783-796.
11. Cabaret J., N. Gasnier, and P. Jacquiet. 1998. Fecal egg counts are representative of digestive-tract strongyle worm burdens in sheep and goats. Parasite 5:137-142.
12. Caron A., P.C. Cross, and J.T. du Toit. 2003. Ecological implications of bovine tuberculosis in African buffalo herds. Ecol Appl 13:1338-1345.
13. Cremer S. and M. Sixt. 2009. Analogies in the evolution of individual and social immunity. Philos Trans R Soc B 364: 129-142.
14. Cross P.C., D.M. Heisey, and J.A. Bowers. 2009. Disease, predation and demography: assessing the impacts of bovine tuberculosis on African buffalo by monitoring at individual and population levels. J Appl Ecol 46:457-465.
15. Davies W.A., V.P. Ackerman, and D.S. Nelson. 1981. Mechanism for nonspecific immunity of Listeria monocytogenes in rats mediated by platelets and the clotting system. Infect Immun 33:477-481.
16. Demas G.E., D.A. Zysling, B.R. Beechler, M.P. Muehlenbein, and S.S. French. 2011. Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. Anim Ecol 80:710-730.
17. du Toit J.T. 2003. Large herbivores and savanna heterogeneity. Pp. 292-309 in H.C. Biggs, J.T. du Toit, K. Johan, K. Rogers, A. Sinclair, and B. Walker, eds. The Kruger experience: ecology and management of savannah heterogeneity. Island, Washington, DC.
18. Ezenwa V.O. 2003. Habitat overlap and gastrointestinal parasitism in sympatric African bovids. Parasitology 126:379-388.
19. Ezenwa V.O., L.S. Ekernas, and S. Creel. 2011a. Unraveling complex associations between testosterone and parasite infection in the wild. Funct Ecol 126:123-140.
20. Ezenwa V.O., R.S. Etienne, G. Luikart, A. Beja-Pereira, and A.E. Jolles. 2011b. Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. Am Nat 176:613-624.
21. Ezenwa V.O. and A.E. Jolles. 2011. From host immunity to pathogen invasion: the effects of helminth coinfection on the dynamics of microparasites. Integr Comp Biol 51:540-551.
22. Ezenwa V.O., A.E. Jolles, and M. O'Brien. 2009. A reliable body condition scoring technique for estimating condition in African buffalo. Afr J Ecol 47:476-481.
23. Fenton A., T. Lamb, and A.L. Graham. 2008. Optimality analysis of Th1/Th2 immune responses during microparasite-macroparasite co-infection, with epidemiological feedbacks. Parasitology 135:841-853.
24. Forsman A.M., L.A. Vogel, S.K. Sakaluk, J.L. Grindstaff, and C.F. Thompson. 2008. Immune-challenged house wren broods differ in the relative strengths of their responses among different axes of the immune system. J Evol Biol 21: 873-878.
25. Freitak D., C. Wheat, D. Heckel, and H. Vogel. 2007. Immune system responses and fitness costs associated with consumption of bacteria in larva of Trichoplusia ni. BMC Biol 5:56.
26. Friedl T.W.P. and R. Edler. 2005. Stress-dependent trade-off between immunological condition and reproductive performance in the polygynous red bishop (Euplectes orix). Evol Ecol 19:221-239.
27. Graham A.L. 2008. Ecological rules governing helminthmicroparasite coinfection. Proc Natl Acad Sci USA 105:566-570.
28. Graham A.L., A.D. Hayward, K.A. Watt, J.G. Pilkington, J.M. Pemberton, and D.H. Nussey. 2011. Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662-665.
29. Graham A.L., T.J. Lamb, A.F. Read, and J.E. Allen. 2005. Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. J Infect Dis 191:410-421.
30. Grasman K.A. 2002. Assessing immunological function in toxicological studies of avian wildlife. Integr Comp Biol 42:34-42.
31. Grenfell B.T. and A.P. Dobson. 1995. Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge.
32. Hanski C., M. Naumann, A. Grutzkau, G. Pluschke, B. Friedrich, H. Hahn, and E.O. Rieckens. 1991. Humoral and cellular defense against intestinal murine infection with Yersinia enterocolitica. Infect Immun 59:1106-1111.
33. Hasselquist D. 2007. Comparative immunoecology in birds: hypotheses and tests. J Ornithol 148:S571-S582.
34. Hawley D.M. and S. Altizer. 2010. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25:48-60.
35. Houston A.I., J.M. McNamara, Z. Barta, and K.C. Klasing. 2007. The effect of energy reserves and food availability on optimal immune defense. Proc R Soc B 274:2835-2842.
36. Jackson J.A., M. Begon, R. Birtles, S. Paterson, I.M. Friberg, A. Hall, A. Lowe, et al. 2011. The analysis of immunological profiles in wild animals: a case study on immunodynamics in the field vole, Microtus agrestis. J Mol Ecol 20:893-909.
37. Jolles A.E. 2007. Population biology of African buffalo (Syncerus caffer) at Hhuhluwe-iMfolozi Park, South Africa. Afr J Ecol 45:398-406.
38. Jolles A.E., D. Cooper, and S.A. Levin. 2005. Hidden effects of chronic tuberculosis in African buffalo. Ecology 86:2358-2364.
39. Jolles A.E., V.O. Ezenwa, R.S. Etienne, W.C. Turner, and H. Off. 2008. Interactions between macroparasites and microparasites drive patterns of infection in free ranging African buffalo. Ecology 89:2239-2240.
40. Klasing K.C. 2004. The costs of immunity. Acta Zool 50:961-969.
41. Lee K.A., M. Wikelski, W.D. Robinson, T.R. Robinson, and K.C. Klasing. 2008. Constitutive immune defences correlate with life-history variables in tropical birds. J Anim Ecol 77: 356-363.
42. Lochmiller R.L. and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
43. Long K.Z. and N. Nanthakumar. 2004. Energetic and nutritional regulation of the adaptive immune response and tradeoffs in ecological immunology. Am J Hum Biol 16:499-507.
44. Martin L.B., D.M. Hawley, and D.R. Ardia. 2011. An introduction to ecological immunology. Funct Ecol 25:1-4.
45. Martin L.B., Z.M. Weil, and R.J. Nelson. 2006. Redefining approaches and diversifying directions in ecoimmunology. Integr Comp Biol 46:1030-1039.
46. Martin L.B., Z.M. Weil, and R.J. Nelson. 2007. Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88:2516-2528.
47. Martin L.B., Z.M. Weil, and R.J. Nelson. 2008. Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans R Soc B 363:321-339.
48. Matson K.D., B.I. Tieleman, and K.C. Klasing. 2006. Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiol Biochem Zool 79: 556-564.
49. Michel A.L., D. Cooper, J. Jooste, L.M. deKlerk, and A.E. Jolles. 2011. Approaches towards optimizing the gamma interferon assay for diagnosing Mycobacterium bovis infection in African buffalo. Prevent Vet Med 98:142-151.
50. Millet S., J. Bennett, K.A. Lee, M. Hau, and K.C. Klasing. 2007. Quantifying and comparing constitutive immunity across avian species. Dev Comp Immunol 31:188-201.
51. Morel P.A. and T.B. Oriss. 1998. Crossregulation between Th1 and Th2 cells. Crit Rev Immunol 18:275-303.
52. Moret Y. and P. Schmid-Hempel. 2001. Entomology: immune defence in bumble-bee offspring. Nature 414:506.
53. Moret Y. and M.T. Siva-Jothy. 2003. Adaptive innate immunity? responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitar. Proc R Soc B 270:2475-2480.
54. Mosmann T.R. and S. Sad. 1996. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17:138-146.
55. Pollock J.M., J.D. Rogers, M.D. Welsh, and J. McNair. 2006. Pathogenesis of bovine tuberculosis: the role of experimental models of infection. Vet Microbiol 112:141-150.
56. Prins H.T. 1996. Ecology and behavior of the African buffalo: social inequality and decision making. Chapman & Hall, London.
57. Raja A. 2004. Immunology of tuberculosis. Indian J Med Res 120:213-232.
58. Sadd B.M. and P. Schmid-Hempel. 2009. Principles of ecoimmunology. Evol Appl 2:113-121.
59. Schiller I.W., R. Waters, H.M. Vordermeier, B. Nonnecke, M. Welsh, N. Keck, A. Whelan, et al. 2009. Optimization of a whole-blood gamma interferon assay for detection of Mycobacterium bovis-infected cattle. Clin Vaccine Immunol 16: 1196-1202.
60. Schulenberg H., J. Kurtz, Y. Moret, and M.T. Siva-Jothy. 2009. Introduction: ecological immunology. Proc R Soc B 364:3-14.
61. Stear M.J., S.J. Bishop, J.L. Duncan, Q.A. McKellar, and M. Murray. 1994. The repeatability of faecal egg counts, peripheral eosinophil counts, and plasma pepsinogen concentrations during deliberate infections with Ostertagia circumcincta. Int J Parasitol 25:375-380.
62. Tieleman B.I., J.B. Williams, R.E. Ricklefs, and K.C. Klasing. 2005. Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc R Soc B 272: 1715-1720.
63. Tizard I. 2004. Veterinary immunology. Saunders, Philadelphia.
64. Wilcoxen T.E., R.K. Boughton, and S.J. Schoech. 2010. Selection on innate immunity and body condition in Florida scrubjays throughout an epidemic. Biol Lett 6:552-554.
65. Wood P.R. and S.L. Jones. 2001. BOVIGAM: an in vitro cellular diagnostic test for bovine tuberculosis. Tuberculosis 81:147-155.