Explaining variance of avian malaria infection in the wild: The importance of host density, habitat, individual life-history and oxidative stress

BMC Ecology

Volumn 13, Issue , 2013, Pages

  Isaksson, Caroline ^a,b   Sepil, Irem ^a   Baramidze, Vladimer ^a   Sheldon, Ben C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Antioxidants; Glutathione; Host density; Hydroperoxides; Oxidative stress; Parus major; Plasmodium

Indexed keywords

ANTIOXIDANT; HOST; IMMUNE RESPONSE; INFECTIOUS DISEASE; LIFE HISTORY; MALARIA; PARASITE; PASSERINE; PHENOTYPE; PHYSIOLOGY;

AVES; PARUS; PARUS MAJOR; PLASMODIUM RELICTUM; PLASMODIUM SP.;

ANIMAL; ECOSYSTEM; HOST PARASITE INTERACTION; MALARIA, AVIAN; METABOLISM; OXIDATIVE STRESS; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM; POPULATION DENSITY; SONGBIRD; SPECIES DIFFERENCE; WILD ANIMAL; ARTICLE; AVIAN MALARIA;

ANIMALS; ANIMALS, WILD; ECOSYSTEM; HOST-PARASITE INTERACTIONS; MALARIA, AVIAN; OXIDATIVE STRESS; PASSERIFORMES; PLASMODIUM; POPULATION DENSITY; SPECIES SPECIFICITY;

EID: 84875864643     PISSN: None     EISSN: 14726785     Source Type: Journal    
DOI: 10.1186/1472-6785-13-15     Document Type: Article

References (66)

1. Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 2007, 16:3263-3273. 10.1111/j.1365-294X.2007.03362.x, 17651202.
2. Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC. Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates. J Anim Ecol 2011, 80:1207-1216. 10.1111/j.1365-2656.2011.01893.x, 21848864.
3. Bensch S, Akesson A. Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 2003, 89:388-391. 10.1645/0022-3395(2003)089[0388:TASVOH]2.0.CO;2, 12760661.
4. Valkiūnas G. Avian malaria parasites and other haemosporidia 2005, CRC Press, Boca Raton.
5. Rogers DJ, Randolph SE. Climate change and vector-borne diseases. Advan Parasitol 2006, 62:345-381.
6. Garamszegi LZ. Climate change increases the risk of malaria in birds. Glob Change Biol 2011, 17:1751-1759.
7. Knowles SCL, Wood MJ, Alves R, Wilkin TA, Bensch S, Sheldon BC. Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol Ecol 2011, 20:1062-1076. 10.1111/j.1365-294X.2010.04909.x, 21073677.
8. Sehgal RNM, Buermann W, Harrigan RJ, Bonneaud C, Loiseau C, Chasar A, Sepil I, Valkiūnas G, Iezhova T, Saatchi S, Smith TB. Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. Proc R Soc B 2010, 278:1025-1033. 3049032, 20880888.
9. Ricklefs RE, Swanson BL, Fallon SM, Martinez-Abrain A, Scheuerlein A, Gray J, Latta SC. Community relationships of avian malaria parasites in southern Missouri. Ecol Monogra 2005, 75:543-559.
10. Duckworth RA, Mendonca MT, Hill GE. A condition dependent link between testosterone and disease resistance in the house finch. Proc R Soc B 2001, 268:2467-2472. 10.1098/rspb.2001.1827, 1088901, 11747565.
11. van de Crommenacker J, Richardson DS, Kolz AM, Hutchings K, Komdeur J. Parasitic infection and oxidative status are associated and vary with breeding activity in the Seychelles warbler. Proc R Soc B 2011, online.
12. Anderson RM, May RM. Population biology of infectious diseases: Part I. Nature 1979, 280:361-367. 10.1038/280361a0, 460412.
13. Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 1996, 11:317-321. 10.1016/0169-5347(96)10039-2, 21237861.
14. Sorci G, Faivre B. Inflammation and oxidative stress in vertebrate host-parasite systems. Phil Trans R Soc B 2009, 364:71-83. 10.1098/rstb.2008.0151, 2666694, 18930878.
15. Knowles SCL, Palinauskas V, Sheldon BC. Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from wild bird population. J Evol Biol 2010, 23:557-569. 10.1111/j.1420-9101.2009.01920.x, 20070458.
16. Knowles SCL, Nakagawa S, Sheldon BC. Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Funct Ecol 2009, 23:405-415.
17. Asghar M, Hasselquist D, Bensch S. Are chronic avian haemosporidian infections costly in wild birds?. J Avian Biol 2011, 42:530-537.
18. Opplinger A, Christe P, Richner H. Clutch size and malaria resistance. Nature 1996, 391:565.
19. LaPointe DA, Atkinson CT, Samuel MD. Ecology and conservation biology of avian malaria. Ann N Y Acad Sci 2011, 1249:211-226.
20. van Riper C, van Riper SGIII, Goff ML, Laird M. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monog 1986, 56:327-344.
21. Yorinks N, Atkinson CT. Effects of malaria (Plasmodium relictum) on activity budgets of experimentally-infected juvenile Apapane (Himatione sanguinea). Auk 2000, 117:731-738.
22. Atkinson CT, Samuel CT. Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on `apapane Himatione sanguinea. J Avian Biol 2010, 41:357-366.
23. Stocker R, Hunt NH, Buffinton GD, Weidemann MJ, Lewis-Hughes PH, Clark IA. Oxidative stress and protective mechanisms in erythocytes in relation to Plasmodium vinckei load. Proc Natl Acad Sci U S A 1985, 82:548-551. 10.1073/pnas.82.2.548, 397077, 3855565.
24. Swindle EJ, Metcalfe DD. The role of reactive oxygen species and nitric oxide in mast cell-dependent inflammatory responses. Immunol Rev 2007, 217:185-205.
25. Goldberg DE. Hemoglobin degradation. Curr Top Microbiol 2005, 295:275-291.
26. Lüersen K, Walter RD, Müller S. Plasmodium falciparum-infected red blood cells depend on a functional glutathione de novo synthesis attributable to an enhanced loss of glutathione. Biochem J 2000, 346:545-552. 10.1042/0264-6021:3460545, 1220884, 10677377.
27. Müller S. Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol Microbiol 2004, 53:1291-1305. 10.1111/j.1365-2958.2004.04257.x, 15387810.
28. Bertrand S, Criscuolo F, Faivre B, Sorci G. Immune activation increases the susceptibility to oxidative tissue damage in zebra finches. Funct Ecol 2006, 20:1022-1027.
29. Monaghan P, Metcalfe NB, Torres R. Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 2009, 12:75-92. 10.1111/j.1461-0248.2008.01258.x, 19016828.
30. Isaksson C, Sheldon BC, Uller T. The challenge of integrating oxidative stress into life-history biology. BioScience 2011, 61:194-202.
31. Cosgrove CL, Wood MJ, Day KP, Sheldon BC. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 2008, 77:540-548. 10.1111/j.1365-2656.2008.01370.x, 18312339.
32. Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC. Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. J Anim Ecol 2011, 80:1196-1206. 10.1111/j.1365-2656.2011.01836.x, 21426343.
33. Tracy RC, Nussear KE, Esque TC, Dean-Bradley K, Tracy CR, DeFalco LA, Castle KT, Zimmerman LC, Espinoza RE, Barber AM. The importance of physiological ecology in conservation biology. Integr Comp Biol 2006, 46:1191-1205. 10.1093/icb/icl054, 21672817.
34. Smith DL, Dushoff J, McKenzie FE. The risk of a mosquito-borne infection in a heterogeneous environment. Pub Lib Sci Biol 2004, 2:e368.
35. Palinauskas V, Valkiunas G, Bolshakov CV, Bensch S. Plasmodium relictum (lineage P-SGS1): Effects on experimentally infected passerine birds. Exp Parasitol 2008, 120:372-380. 10.1016/j.exppara.2008.09.001, 18809402.
36. Kimura M, Darbro JM, Harrington LC. Avian malaria parasites share congeneric mosquito vectors. J Parasitol 2010, 96:144-151. 10.1645/GE-2060.1, 19697968.
37. Ortego J, Cordero PJ. Factors associated with the geographic distribution of leucocytozoa parasitizing nestling eagle owls (Bubo bubo): a local spatial-scale analysis. Conserv Genet 2010, 11:1479-1487.
38. Beaudoin RL, Applegate JE, David DE, McLean RG. A model for the ecology of avian malaria. J Wildl Dis 1971, 7:5-13.
39. Sol D, Jovani R, Torres J. Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 2003, 135:542-547.
40. Mattson MP. Hormesis defined. Ageing Res Rev 2008, 7:1-7. 10.1016/j.arr.2007.08.007, 2248601, 18162444.
41. McCurdy DG, Shutler D, Mullie A, Forbes MR. Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 1998, 82:303-312.
42. Christe P, Glaizot O, Strepparava N, Devevey G, Fumagalli L. Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress. Proc R Soc B 2011, online.
43. Bray PG, Ward SA, O'Neill PM. Quinolines and artemisinin: chemistry, biology and history. Curr Top Microbiol 2005, 295:3-38.
44. Francis SE, Sullivan DJ, Goldberg DE. Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Ann Rev Microbiol 1997, 51:97-123.
45. Schwarzer E, Kühn H, Valente E, Arese P. Malaria-parasitized erythorocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions. Blood 2003, 101:722-728. 10.1182/blood-2002-03-0979, 12393662.
46. Meister A, Anderson ME. Glutathione. Ann Rev Biochem 1983, 52:711-760. 10.1146/annurev.bi.52.070183.003431, 6137189.
47. Chandra R, Tripathi LM, Saxena JK, Puri SK. Implication of intracellular glutathione and its related enzymes on resistance of malaria parasites to the antimalarial drug arteether. Parasitol Int 2011, 60:97-100. 10.1016/j.parint.2010.09.009, 20971213.
48. Costantini D, Verhulst S. Does high anti-oxidant capacity indicate low oxidative stress?. Funct Ecol 2009, 23:506-509.
49. Alonso-Alvarez C, Perez-Rodriguez L, Garcia JT, Viñuela J, Mateo R. Age and breeding effort as sources of individual variability in oxidative stress markers in a bird species. Physiol Biochem Zoo 2010, 83:110-118.
50. Eckman JR, Eaton JW. Dependence of plasmodial glutathione metabolism on the host cell. Nature 1979, 278:754-756. 10.1038/278754a0, 34799.
51. Patzewitz E-M, Wong EH, Müller S. Dissecting the role of gluthathione biosynthesis in Plasmodium falciparum. Mol Microbiol 2012, 83:304-318. 10.1111/j.1365-2958.2011.07933.x, 3321222, 22151036.
52. Perrins CM. Tits and their caterpillar food supply. Ibis 1991, 133:49-54.
53. Lin S-K, Tsai S-M, Huang J-C, Lee S-C, Wu S-H, Wu S-H, Ma H, Lin J-T, Tsai L-Y. Effects of storage time and temperature on the stability of glutathione in deproteinized blood sample. J Food Drug Anal 2006, 14:141-146.
54. Becker K, Tilley L, Vennerstrom JL, Roberts D, Rogerson S, Ginsburg H. Oxidative stress in malaria parasite-infected erythrocytes: host - parasite interactions. Int J Parasitol 2004, 34:163-189. 10.1016/j.ijpara.2003.09.011, 15037104.
55. Halliwell B, Gutteridge JMC. Free radicals in biology and medicine 2002, Clarendon Press, Oxford.
56. Baker MA, Cerniglia GJ, Zaman A. Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 1990, 190:360-365. 10.1016/0003-2697(90)90208-Q, 2291479.
57. Vandeputte C, Guizon I, Genestiedenis I, Vannier B, Lorenzon G. A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells - performance study of a new miniaturized protocol. Cell Biol Toxicol 1994, 10:415-421. 10.1007/BF00755791, 7697505.
58. Isaksson C, Örnborg J, Stephensen E, Andersson S. Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits. Ecohealth 2005, 2:138-146.
59. Costantini D, Dell'Omo G. Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol A 2006, 145:137-142.
60. van de Crommenacker J, Komdeur J, Burke T, Richardson DS. Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis). J Anim Ecol 2011, 80:668-680. 10.1111/j.1365-2656.2010.01792.x, 3107423, 21198588.
61. Palacios MG, Cunnick JE, Winkler DW, Vleck CM. Immunosenescence in some but not all immune components in a free-living vertebrate, the tree swallow. Proc R Soc B 2007, 274:951-957. 10.1098/rspb.2006.0192, 2141670, 17251097.
62. Quinn G, Keough M. Experimental design and data analysis for biologists 2002, Cambridge University Press, Cambridge.
63. Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach 2002, Springer, New York.
64. Burnham KP, Anderson DR, Huyvaert KP. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 2011, 65:23-35.
65. Symonds MRE, Moussalli A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav Ecol Sociobiol 2011, 65:13-21.
66. R Development Core Team R: A language and environment for statistical computing 2011, R Foundation for Statistical Computing, Vienna, Austria, URL http://www.R-project.org/, R Development Core Team.