Abstract
We studied the consequences of chronic infections by three different lineages of avian malaria, two Plasmodium (RTSR1, LK6) and one Haemoproteus (LK2), on reproductive performance of Lesser Kestrels (Falco naumanni). Malaria infections in male and female parents had no effect on clutch size, hatching success or nesting success. However, when only successful nests were considered, we found that males parasitized by LK6 raised a lower number of fledglings, suggesting that the level of parental effort by males may be limited by this particular lineage of Plasmodium. This effect was not evident in females, probably due to the higher investment of males during the chick rearing period in this species. Overall, we have found that chronic stages of specific malaria lineages have certain negative consequences on host reproductive performance, highlighting the importance of considering genetic differences among malaria parasites to study their consequences on natural bird populations.
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References
Aparicio JM (1997) Costs and benefits of surplus offspring in the lesser kestrel (Falco naumanni). Behav Ecol Sociobiol 41:129–137
Aparicio JM, Bonal R (2002) Effects of food supplementation and habitat selection on timing of lesser kestrel breeding. Ecology 83:873–877
Aparicio JM, Cordero PJ (2001) The effects of the minimum threshold condition for breeding on offspring sex-ratio adjustment in the lesser kestrel. Evolution 55:1188–1197
Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii amakihi. J Wildl Dis 36:197–204
Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, JhalaYV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proc R Soc Lond B 273:2935–2944
Bensch S, Perez-Tris J, Waldenstrom J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58:1617–1621
Bensch S, Stjernman M, Hasselquist D et al (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
Bensch S, Waldenstrom J, Jonzen N et al (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122
Biber JP (1990) Action plan for the conservation of western lesser kestrel Falco naumanni populations. ICBP, Cambridge
Bolton M, Monaghan P, Houston DC (1991) An improved technique for estimating pectoral muscle protein condition from body measurements of live gulls. Ibis 133:264–270
Dawson RD, Bortolotti GR (2000) Effects of hematozoan parasites on condition and return rates of American kestrels. Auk 117:373–380
Dawson RD, Bortolotti GR (2001) Sex-specific associations between reproductive output and hematozoan parasites of American kestrels. Oecologia 126:193–200
de Roode JC, Helinski MEH, Anwar MA, Read AF (2005) Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am Nat 166:531–542
Fallon SM, Bermingham E, Ricklefs RE (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. Am Nat 165:466–480
Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717
Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78
Garvin MC, Homer BL, Greiner EC (2003) Pathogenicity of Haemoproteus danilewskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). J Wildl Dis 39:161–169
Gosler AG, Harper D (2000) Assessing the heritability of body condition in birds: a challenge exemplified by the great tit Parus major L. (Aves). Biol J Linn Soc 71:103–117
Green RH (1979) Sampling design and statistical methods for environmental biologists. Wiley, New York
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387
Hellgren O (2005) The occurrence of haemosporidian parasites in the Fennoscandian bluethroat (Luscinia svecica) population. J Ornithol 146:55–60
Jarvi SI, Schultz JJ, Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88:153–158
Jarvi SI, Farias MEM, Baker H, Freifeld HB, Baker PE, Van Gelder E, Massey JG, Atkinson CT (2003) Detection of avian malaria (Plasmodium spp.) in native land birds of American Samoa. Conserv Gen 4:629–637
Korpimäki E, Hakkarainen H, Bennett GF (1993) Blood parasites and reproductive success of tengmalm owls—detrimental effects on females but not on males. Funct Ecol 7:420–426
Krackow S, Tkadlec E (2001) Analysis of brood sex ratios: implications of offspring clustering. Behav Ecol Sociobiol 50:293–301
Kruuk LEB, Sheldon BC, Merila J (2002) Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc R Soc Lond B 269:1581–1589
Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 267:2507–2510
Newton SF (1993) Body condition of a small passerine bird—ultrasonic assessment and significance in overwinter survival. J Zool 229:561–580
Ortego J, Calabuig G, Cordero PJ, Aparicio JM (2007a) Genetic characterization of avian malaria (Protozoa) in the endangered lesser kestrel, Falco naumanni. Parasitol Res 101:1153–1156
Ortego J, Calabuig G, Cordero PJ, Aparicio JM (2007b) Egg production and individual genetic diversity in lesser kestrels. Mol Ecol 16:2383–2392
Ortego J, Cordero PJ, Aparicio JM, Calabuig G (2007c) No relationship between individual genetic diversity and prevalence of avian malaria in a migratory kestrel. Mol Ecol 16:4858–4866
Ortego J, Aparicio JM, Calabuig G, Cordero PJ (2007d) Increase of heterozygosity in a growing population of lesser kestrels. Biol Lett 3:585–588
Pérez-Tris J, Hellgren O, Križanauskienė A, Waldenström J, Secondi J, et al. (2007) Within-host speciation of malaria parasites. PLoS ONE 2(2):e235. doi:https://doi.org/10.1371/journal.pone.0000235
Perrins CM (1970) The timing of birds’ breeding seasons. Ibis 112:242–255
Poulin R, Marshall LJ, Spencer HG (2000) Genetic variation and prevalence of blood parasites do not correlate among bird species. J Zool 252:381–388
Reid JM, Arcese P, Keller LF (2003) Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects. Proc R Soc Lond B 270:2151–2157
Ricklefs RE, Swanson BL, Fallon SM, Martínez-Abraín A, Scheuerlein A, Gray J, Latta SC (2005) Community relationships of avian malaria parasites in Southern Missouri. Ecol Mon 75:543–559
SAS Institute (2004) SAS/STAT 9.1 user’s guide. SAS Institute, Cary
Sol D, Jovani R, Torres J (2003) Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 135:542–547
Tella JL, Forero MG, Gajon A, Hiraldo F, Donazar JA (1996) Absence of blood-parasitization effects on lesser kestrel fitness. Auk 113:253–256
Tomás G, Merino S, Martinez J, Moreno J, Sanz JJ (2005) Stress protein levels and blood parasite infection in blue tits (Parus caeruleus): a medication field experiment. Ann Zool Fenn 42:45–56
Van Riper C, Vanriper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in hawaiian land birds. Ecol Mon 56:327–344
Waldenström J, Bensch S, Hasselquist D, Ostman O (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90:191–194
Westerdahl H, Waldenstrom J, Hansson B et al (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B 272:1511–1518
Acknowledgments
This manuscript was greatly improved by the comments of Robert E. Ricklefs and an anonymous reviewer. This work received financial support from the projects: CGL2005-05611-C02-02/BOS (Ministerio de Educación Ciencia) and PAI05-053 (Junta de Comunidades de Castilla-La Mancha). During this work J.O and G.C. were supported by predoctoral fellowships from the Junta de Comunidades de Castilla-La Mancha and the European Social Fund. We performed all the laboratory work at the Laboratory of Genetics of the IREC and sequencing was performed by the Centro de Investigaciones Biológicas (CSIC) of Madrid. We manipulated and banded Lesser Kestrels under license from the Spanish institutional authorities (Environmental Agency of the Community of Castilla-La Mancha and the Ringing Office of the Ministry of Environment) and we followed general ethical guidelines for animal welfare and nature conservation.
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Communicated by F. Bairlein.
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Ortego, J., Cordero, P.J., Aparicio, J.M. et al. Consequences of chronic infections with three different avian malaria lineages on reproductive performance of Lesser Kestrels (Falco naumanni). J Ornithol 149, 337–343 (2008). https://doi.org/10.1007/s10336-008-0287-9
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DOI: https://doi.org/10.1007/s10336-008-0287-9