Comparative analysis reveals a possible immunity-related absence of blood parasites in Common Gulls (Larus canus) and Black-headed Gulls (Chroicocephalus ridibundus)

Journal of Ornithology

Volumn 153, Issue 4, 2012, Pages 1245-1252

  Krams, Indrikis ^a   Suraka, Valerija ^b,c   Rattiste, Kalev ^d   Aboliņš Abols, Mikus ^e   Krama, Tatjana ^c   Rantala, Markus J ^f   Mierauskas, Pranas ^g   Cirule, Dina ^b,c   Saks, Lauri ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b INSTITUTE OF FOOD SAFETY   (Latvia)

^c DAUGAVPILS UNIVERSITY   (Latvia)

^d ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^e INDIANA UNIVERSITY   (United States)

^f UNIVERSITY OF TURKU   (Finland)

^g MYKOLAS ROMERIS UNIVERSITY   (Lithuania)

Author keywords

Blood parasites; Ecological immunology; Gulls; Haematozoa; Lack of parasites

Indexed keywords

COMPARATIVE STUDY; HEMOPARASITE; HOST-PARASITE INTERACTION; IMMUNITY; PARASITE PREVALENCE; WADER;

AVES; LARUS CANUS; LARUS RIDIBUNDUS;

EID: 84866461927     PISSN: 21937192     EISSN: 21937206     Source Type: Journal    
DOI: 10.1007/s10336-012-0859-6     Document Type: Article

References (93)

1. Allander K, Bennett GF (1994) Prevalence and intensity of haematozoan infection in a population of great tits Parus majorr from Gotland, Sweden. J Avian Biol 25(1): 69-74.
2. Atkinson CT, Forrester DJ, Greiner EC (1988) Pathogenicity of Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys. J Parasitol 74(2): 228-239.
3. Atkinson CT, Dusek RJ, Lease JK (2001) Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii Amakihi. J Wildl Dis 37(1): 20-27.
4. Bennett G (1993) Phylogenetic distribution and possible evolution of the avian species of the Haemoproteidae. Syst Parasitol 26(1): 39-44.
5. Bennett GF, Earle RA, Du Toit H, Huchzermeyer FW (1992a) A host-parasite catalogue of the haematozoa of the Sub-Saharan birds. J Vet Res 59(1): 1-73.
6. Bennett GF, Montgomere R, Seutin G (1992b) Scarcity of haematozoa in birds breeding on the Arctic tundra of North America. Condor 94: 289-292.
7. Bennett G, Peirce M, Earle RA (1994) An annotated checklist of the valid avian species of Haemoproteus, Leucocytozoon (Apicomplexa: Haemosporida) and Hepatozoon (Apicomplexa: Haemogregarinidae). Syst Parasitol 29(1): 61-73.
8. Bennett GF, Squiresparsons D, Siikamäki P, Huhta E, Allander K, Hillström L (1995) A comparison of the blood parasites of three Fenno-Scandian populations of the Pied Flycatcher Ficedula hypoleuca. J Avian Biol 26(1): 33-38.
9. Bensch S, Stjernman M, Hasselquist D, Östman Ö, Hansson B, Westerdahl H, Torres-Pinheiro R (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267: 1583-1589.
10. Blanco G, Gajon A, Doval G, Martínez F (1998) Absence of blood parasites in Griffon vultures from Spain. J Wildl Dis 34(3): 640-643.
11. Bosch M, Figuerola J et al (1997) Intracolonial differences in the infestation by Haemoproteus lari on yellow-legged gulls Larus cachinnans. Ornis Fenn 74: 105-112.
12. Bukacinski D, Bukacinska M (2000) The impact of mass outbreaks of black flies (Simuliidae) on the parental behaviour and breeding output of colonial common gulls (Larus canus). Ann Zool Fenn 37(1): 43-49.
13. Clayton DH, Moore J (1997) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford.
14. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205: 489-511.
15. Earle RA, Underhill LG (1993) Absence of haematozoa in some Charadriiformes breeding in the Taimyr Peninsula, Russia. Ardea 81: 21-24.
16. Engstrom H, Dufva R et al (2000) Absence of haematozoa and ectoparasites in a highly sexually ornamented species, the crested auklet. Waterbirds 23(3): 486-488.
17. Engstrom H, Dufva R et al (2001) Absence of haematozoa and ectoparasites in a highly sexually ornamented species, the crested auklet. Waterbirds 23(3): 486-488.
18. Esparza B, Martinez-Abrain A et al (2004) Immunocompetence and the prevalence of haematozoan parasites in two long-lived seabirds. Ornis Fenn 81(1): 40-46.
19. Figuerola J (1999) Effects of salinity on rates of infestation of waterbirds by haematozoa. Ecography 22(6): 681-685.
20. Figuerola J, Velarde R et al (1996) Absence of haematozoa in a breeding population of Kentish plover Charadrius alexandrinus in northeast Spain. J Fur Ornithol 137(4): 523-525.
21. Fokidis BH, Greiner EC et al (2008) Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J Avian Biol 39(3): 300-310.
22. Forero MG, Tella JL et al (1997) Absence of blood parasites in the red-necked nightjar. J Field Ornithol 68(4): 575-579.
23. Garvin MC, Greiner EC (2003) Epizootiology of Haemoproteus danilewskyi (Haemosporina: Haemoproteidae) in blue jays (Cyanocitta cristata) in Southcentral Florida. J Wildl Dis 39(1): 1-9.
24. Garvin MC, Homer BL et al (2003) Pathogenicity of Haemoproteus danilewskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). J Wildl Dis 39(1): 161-169.
25. Godfrey DA, Carlson L et al (1987) Quantitative inter-strain comparison of the distribution of choline acetyltransferase activity in the rat cochlear nucleus. Hear Res 31(3): 203-209.
26. Gonzalez-Solis J, Abella JC (1997) Negative record of haematozoan parasites on Cory's shearwater Calonectris diomedea. Ornis Fenn 74(3): 153-155.
27. Greiner EC, Bennett GF et al (1975) Distribution of the avian hematozoa of North America. Can J Zool 53(12): 1762-1787.
28. Hellgren O, Waldenström J et al (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90(4): 797-802.
29. Hellgren O, Bensch S et al (2008) Bird hosts, blood parasites and their vectors-associations uncovered by molecular analyses of blackfly blood meals. Mol Ecol 17(6): 1605-1613.
30. Hõrak P, Ots I et al (1998) Haematological health state indices of reproducing great tits: a response to brood size manipulation. Funct Ecol 12(5): 750-756.
31. Ilmonen P, Hakkarainen H et al (1999) Parental effort and blood parasitism in Tengmalm's owl: effects of natural and experimental variation in food abundance. Oikos 86(1): 79-86.
32. Isobe T, Suzuki K (1987) Immunoglobulin M and G immune response to Leucocytozoon caulleryi in chickens. Jpn J Vet Sci 49(2): 333-339.
33. Jarvi SI, Schultz JJ et al (2002) PCR Diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88(1): 153-158.
34. Jones HI, Shellam GR (1999) The occurrence of blood-inhabiting protozoa in captive and free-living penguins. Polar Biol 21(1): 5-10.
35. Jovani R, Tella JL et al (2001) Apparent absence of blood parasites in the patagonian seabird community: Is it related to the marine environment? Waterbirds 24(3): 430-433.
36. Jovani R, Tella JL et al (2002) Absence of haematozoa on colonial white storks Ciconia ciconia throughout their distribution range in Spain. Ornis Fenn 79(1): 41-44.
37. Knowles SCL, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23: 557-569.
38. Lardeux FJR, Ottenwaelder T (1997) Density of larval Culicoides belkini (Diptera: Ceratopogonidae) in relation to physicochemical variables in different habitats. J Med Entomol 34(4): 387-395.
39. Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9(1): 8-13.
40. Little RM, Earle RA (1994) Lack of avian haematozoa in the Phasianinae of Robben Island. Ostrich 65: 343-344.
41. Little RM, Earle RA (1995) Sandgrouse (Pterocleidae) and sociable weavers Philetarius socius lack avian haematozoa in semi-arid regions of South Africa. J Arid Environ 30(3): 367-370.
42. Loye JE, Zuk M (1991) Bird-parasite interactions. Ecology, evolution and behaviour. Oxford University Press, Oxford.
43. Martinez-Abrain A, Urios G (2002) Absence of blood parasites in nestlings of the Eleonora's falcon (Falco eleonorae). J Raptor Res 36(2): 139-141.
44. Martinez-Abrain A, Merino S et al (2002) Prevalence of blood parasites in two western-Mediterranean local populations of the yellow-legged gull Larus cachinnans michahellis. Ornis Fenn 79(1): 34-40.
45. Martinez-Abrain A, Esparza B et al (2004) Lack of blood parasites in bird species: does absence of blood parasite vectors explain it all? Ardeola 51(1): 225-232.
46. Marzal A, Lope Fd et al (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142(4): 541-545.
47. Masello JF, Choconi RG et al (2006) Blood and intestinal parasites in wild Psittaciformes: a case study of burrowing parrots (Cyanoliseus patagonus). Ornitologia Neotropical 17(4): 515-529.
48. Massey JG, Graczyk TK et al (1996) Characteristics of naturally acquired Plasmodium relictum capistranoae infections in naive Hawaiian crows (Corvus hawaiiensis) in Hawaii. J Parasitol 82(1): 182-185.
49. Merino S, Minguez E (1998) Absence of haematozoa in a breeding colony of the storm petrel Hydrobates pelagicus. Ibis 140(1): 180-181.
50. Merino S, Barbosa A et al (1997) Absence of haematozoa in a wild chinstrap penguin Pygoscelis antarctica population. Polar Biol 18(3): 227-228.
51. Merino S, Moreno J et al (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 267(1461): 2507-2510.
52. Merino S, Moreno J et al (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Aust Ecol 33(3): 329-340.
53. Möller AP (ed) (1997) Parasitism and the evolution of host life history. Host-parasite evolution. Oxford University Press, New York.
54. Morales J, Moreno J et al (2004) Associations between immune parameters, parasitism, and stress in breeding pied flycatcher (Ficedula hypoleuca) females. Can J Zool 82(9): 1484-1492.
55. Onno S (1968) The life span of the common gull and the age structure of its population in Estonia. Commun Baltic Comm Study Bird Migration 5: 81-109.
56. Ots I, Hõrak P (1998) Health impact of blood parasites in breeding great tits. Oecologia 116(4): 441-448.
57. Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2011) Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Exp Parasitol 127: 527-533.
58. Peirce MA (1981a) Distribution and host-parasite checklist of the Hematozoa of birds in Western Europe. J Nat Hist 15(3): 419-458.
59. Peirce MA (1981b) Haematozoa of British birds: VI. Redescription of Haemoproteus larae Yakunin from the lesser black-backed gull Larus fuscus. Taylor & Francis, London.
60. Peirce MA, Brooke M (1993) Failure to detect blood parasites in seabirds from the Pitcairn Islands. Seabird 15: 72-75.
61. Peirce MA, Prince PA (1980) Hepatozoon albatrossisp. Nov (Eucoccida : Hepatozoidae) from Diomedea spp. in the Antarctic. J Nat Hist 14(3): 447-452.
62. Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure. Oikos 80: 623-631.
63. Quillfeldt P, Martinez J et al (2010) Hemosporidian blood parasites in seabirds-a comparative genetic study of species from Antarctic to tropical habitats. Naturwissenschaften 97(9): 809-817.
64. Quillfeldt P, Arriero E et al (2011) Prevalence of blood parasites in seabirds-a review. Front Zool 8(1): 26.
65. Randi E, Spina F (1987) an electrophoretic approach to the systematics of italian gulls and terns (aves, laridae and sternidae). Ital J Zool 21(4): 317-344.
66. Rattiste K (1983) Distribution of the West-Estonian common gull Larus canus in the non-breeding period. Ornis Fenn Suppl 3: 616-62.
67. Rattiste K, Lilleleht V (1986) Some aspects of the demography of the common gull (Larus canus) in Estonia. Baltic Birds IV. In: Proceedings of the fourth conference on the study and conservation of migratory birds of the baltic basin, Frostavallen, Sweden, Sveriges Ornitologiska Förening.
68. Rattiste K, Lilleleht V (1995) Survival rates of breeding common gulls in Estonia. J Appl Stat 22(5-6): 1057-1062.
69. Ricklefs RE (1992) Embryonic development period and the prevalence of avian blood parasites. Proc Nat Acad Sci USA 89(10): 4722-4725.
70. Ricklefs RE, Fallon SM (2001) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B 269(1494): 885-892.
71. Ricklefs RE, Swanson BL, Fallon SM, Martinez-Abrain A, Scheuerlein A, Gray J, Latta SC (2005) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75: 543-559.
72. Ruiz X, Oro D et al (1995) Incidence of a Haemoproteus lari parasitemia in a threatened gull: Larus audouinii. Ornis Fenn 72(4): 159-164.
73. Rytkönen S, Ilomaki K et al (1996) Absence of blood parasites in willow tits Parus montanus in northern Finland. J Avian Biol 27(2): 173-174.
74. Sanz JJ, Arriero E et al (2001) Female hematozoan infection reduces hatching success but not fledging success in pied flycatchers Ficedula hypoleuca. Auk 118(3): 750-755.
75. Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, Oxford.
76. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11: 317-321.
77. Sol D, Jovani R et al (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23(3): 307-314.
78. Sorci G (1995) Repeated measurments of blood parasite levels reveal limited ability for host recovery in the common lizard (Lacerta vivipara). J Parasitol 81(5): 825-827.
79. Spungis V (2000) A cbecklist of Latvian mosquitoes (Diptera, Culicidae). Eur Mosquito Bull 6: 8-11.
80. Spuris Z (1974) Divsparņi - Diptera. In: Spuris Z (ed) Latvijas dzivnieku pasaule. Liesma, Riga.
81. Stewart IRK, Ringsby TH et al (1997) Absence of haematozoa in passerines from a Norwegian archipelago. Ornis Fenn 74(4): 201-203.
82. Tella JL, Gortazar C et al (1995) Apparent lack of effects of a high lousefly infestation (Diptera, Hippoboscidae) on adult colonial alpine swifts. Ardea 83: 435-439.
83. Tella JL, Forero MG et al (1996) Absence of blood-parasitization effects on lesser kestrel fitness. Auk 113(1): 253-256.
84. Tella JL, Blanco G et al (1999) Habitat, world geographic range, and embryonic development of hosts explain the prevalence of avian hematozoa at small spatial and phylogenetic scales. Proc Nat Acad Sci USA 96(4): 1785-1789.
85. Temple SA (1987) Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68(3): 669-674.
86. Tomas G, Merino S et al (2005) Stress protein levels and blood parasite infection in blue tits (Parus caeruleus): a medication field experiment. Ann Zool Fenn 42(1): 45-56.
87. Valera F, Carrillo CM et al (2003) Low prevalence of haematozoa in trumpeter finches Bucanetes githagineus from south-eastern Spain: additional support for a restricted distribution of blood parasites in arid lands. J Arid Environ 55(2): 209-213.
88. Valkiūnas G (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Mol Ecol 20: 3084-3086.
89. Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca Raton.
90. Valkiūnas G, Bensch S et al (2006) Nested cytochrome b PCR diagnostics underestimate mixed infections of avian blood hemosporidian parasites: microscopy is still essential. J Parasitol 92: 418-422.
91. van Riper C III, Atkinson CT et al (1994) Plasmodia of birds. In: Kreier JP (ed) Parasitic protozoa. Academic, San Diego, pp 73-140.
92. Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled. Cambridge University Press, Cambridge.
93. Zuk M, Stoehr AM (2002) Immune defense and host life history. University of Chicago Press, Chicago.