Abstract
The Chernobyl catastrophe provides a rare opportunity to study the ecological and evolutionary consequences of low-level, environmental radiation on living organisms. Despite some recent studies about negative effects of environmental radiation on macroorganisms, there is little knowledge about the effect of radioactive contamination on diversity and abundance of microorganisms. We examined abundance patterns of total cultivable bacteria and fungi and the abundance of feather-degrading bacterial subset present on feathers of barn swallows (Hirundo rustica), a colonial migratory passerine, around Chernobyl in relation to levels of ground level environmental radiation. After controlling for confounding variables, total cultivable bacterial loads were negatively correlated with environmental radioactivity, whereas abundance of fungi and feather-degrading bacteria was not significantly related to contamination levels. Abundance of both total and feather-degrading bacteria increased with barn swallow colony size, showing a potential cost of sociality. Males had lower abundance of feather-degrading bacteria than females. Our results show the detrimental effects of low-level environmental radiation on total cultivable bacterial assemblage on feathers, while the abundance of other microorganism groups living on barn swallow feathers, such as feather-degrading bacteria, are shaped by other factors like host sociality or host sex. These data lead us to conclude that the ecological effects of Chernobyl may be more general than previously assumed and may have long-term implications for host–microbe interactions and overall ecosystem functioning.
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Achá SJ, Kühn I, Mbazima G, Colque-Navarro P, Möllby (2005) Changes of viability and composition of the Escherichia coli flora in faecal samples during long time storage. J Microbiol Meth 63:229–238
Bisson IA, Marra PP, Burtt EH Jr, Sikaroodi M, Gillevet PM (2007) A molecular comparison of plumage and soil bacteria across biogeographic, ecological, and taxonomic scales. Microb Ecol 54:65–81
Bisson IA, Marra PP, Burtt EH Jr, Sikaroodi M, Gillevet PM (2009) Variation in plumage microbiota depends on season and migration. Microb Ecol 58:212–220
Bonisoli-Alquati A, Mousseau TA, Møller AP, Caprioli M, Saino N (2010) Increased oxidative stress in barn swallows from the Chernobyl region. Comp Biochem Physiol A 155:205–210
Brook I (1999) Bacterial interference. Crit Rev Microbiol 25:155–172
Burtt EH Jr, Ichida JM (1999) Occurrence of feather-degrading bacilli in the plumage of birds. Auk 116:364–372
Burtt EH Jr, Ichida JM (2004) Gloger’s rule, feather-degrading bacteria, and color variation among song sparrows. Condor 106:681–686
Caillet S, Millette M, Dussault D, Shareck F, Lacroix M (2008) Effect of gamma radiation on heat shock protein expression of four foodborne pathogens. J Appl Microbiol 105:1384–1391
Clayton DH, Cotgreave P (1994) Relationship of bill morphology to grooming behaviour in birds. Anim Behav 47:195–201
Dadachova E, Bryan RA, Huang X, Moadel T, Schweitzer AD, Aisen P, Nosanchuk JD, Casadevall A (2007) Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS ONE 5:e457
Dadachova E, Casadevall A (2008) Ionizing radiation: how fungi cope, adapt and exploit with the help of melanin. Curr Opin Microbiol 11:525–531
Dehorty BA, Tirabasso PA (2000) Antibiosis between ruminal bacteria and ruminal fungi. Appl Environ Microbiol 66:2921–2927
Dighton J, Tugay T, Zhdanova N (2008) Fungi and ionizing radiation from radionuclides. FEMS Microbiol Lett 281:109–120
Ellegren H, Lindgren G, Primmer CR, Møller AP (1997) Fitness loss and germline mutations in barn swallows breeding in Chernobyl. Nature 389:593–596
European Union (1998) Atlas of caesium deposition on Europe after the Chernobyl accident. EU Publication EUR 16733, Bruxelles, Belgium
Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483
Gunderson AR, Forsyth MH, Swaddle JP (2009) Evidence that plumage bacteria influence feather coloration and body condition of eastern bluebirds Sialis sialis. J Avian Biol 40:440–447
Horrocks N, Perrins C, Charmantier A (2009) Seasonal change in male and female bill knob size in the mute swan Cygnus olor. J Avian Biol 40:511–519
Hubálek Z (1978) Coincidence of fungal species associated with birds. Ecology 59:438–442
Jacob J, Eigener U, Hoppe U (1997) The structure of preen gland waxes from pelecaniform birds containing 3, 7-dimethyloctan-1-ol: an active ingredient against dermatophytes. Zeit Naturforsch C52:114–123
Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67
JMP 5.0.1 (2002) JMP. SAS Institute, Cary
Kovalchuk O, Dubrova YE, Arkhipov A, Hohn B, Kovalchuk I (2000) Wheat mutation rate after Chernobyl. Nature 407:583–584
Lucas FS, Broennimann O, Febbraro I, Heeb P (2003) High diversity among feather-degrading bacteria from a dry meadow soil. Microb Ecol 45:282–290
Lucas FS, Moureau B, Jourdie V, Heeb P (2005) Brood size modifications affects plumage bacterial assemblages of European starlings. Mol Ecol 14:639–646
Mennerat A, Mirleau P, Blondel J, Perret P, Lambrechts MM, Heeb P (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161:849–855
Mironenko NV, Alekhina IA, Zhdanova NN, Bulat SA (2000) Intraspecific variation in gamma-radiation resistance and genomic structure in the filamentous fungus Alternaria alternate: a case study of strains inhabiting Chernobyl reactor nr. 4. Ecotoxicol Environ Saf 45:177–187
Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, Oxford
Møller AP (2002) Developmental instability and sexual selection in stag beetles from Chernobyl and control area. Ethology 108:193–204
Møller AP, Allander K, Dufva R (1993) Parasites and the evolution of host social behavior. Adv Study Behav 22:65–102
Møller AP, Czirják GÁ, Heeb P (2009) Feather micro-organisms and uropygial anti-microbial defenses in a colonial passerine bird. Funct Ecol 23:1097–1102
Møller AP, Hobson KA, Mousseau TA, Peklo AM (2006) Chernobyl as a population sink for barn swallows: tracking dispersal using stable-isotope profiles. Ecol Appl 16:1696–1705
Møller AP, Mousseau TA (2001) Albinism and phenotype of barn swallows Hirundo rustica from Chernobyl. Evolution 55:2097–2104
Møller AP, Mousseau TA (2006) Biological consequences of Chernobyl: 20 years on. Trends Ecol Evol 21:200–207
Møller AP, Mousseau TA (2007) Species richness and abundance of forest birds in relation to radiation at Chernobyl. Biol Lett 3:483–486
Møller AP, Mousseau TA (2009) Reduced abundance of raptors in radioactively contaminated areas near Chernobyl. J Ornithol 150:239–246
Møller AP, Mousseau TA (2009) Reduced abundance of insects and spiders linked to the radiation at Chernobyl 20 years after the accident. Biol Lett 5:356–359
Møller AP, Mousseau TA, Milinevski G, Peklo A, Pysanets E, Szép T (2005) Condition, reproduction and survival of barn swallows from Chernobyl. J Anim Ecol 74:1102–1111
Møller AP, Szép T (2002) Survival rate of adult barn swallows Hirundo rustica in relation to sexual selection and reproduction. Ecology 83:2220–2228
Moysich KB, Menezes RJ, Michalek AM (2002) Chernobyl-related ionizing exposure and cancer risk; an epidemiological review. Lancet Oncol 3:269–279
Petridou E, Trichopoulos D, Dessypris N, Flytzani V, Haidas S, Kalmanti M, Koliouskas D, Kosmidis H, Piperopoulou F, Tzortzatou F (1996) Infant leukaemia after in utero exposure to radiation from Chernobyl. Nature 382:352–353
Pugh GJF (1972) The contamination of birds’ feathers by fungi. Ibis 114:172–177
Revis HC, Waller DA (2004) Bactericidal and fungicidal activity of ant chemicals on feather parasites: an evaluation of anting behavior as a method of self-medication in songbirds. Auk 121:1262–1268
Romanovskaya VA, Rokitko PV, Malashenko YuR, Krishtab TP, Chernaya NA (1999) Sensitivity of soil bacteria isolated from the alienated zone around the Chernobyl Nuclear Power Plant to various stress factors. Microbiol 68:465–469
Romanovskaya VA, Rokitko PV, Mikheev AN, Gushcha NI, Malashenko YuR, Chernaya NA (2002) The effect of γ-radiation and desiccation on the viability of the soil bacteria isolated from the alienated zone around the Chernobyl Nuclear Power Plant. Microbiol 71:608–613
Romanovskaya VA, Sokolov IG, Rokitko PV, Chernaya NA (1998) Effect of radioactive contamination on soil bacteria in the 10-km zone around the Chernobyl Nuclear Power Plant. Microbiol 67:274–280
Romanovskaya VA, Stolyar SM, Malashenko YuR, Shatokima EF (1996) The effect of prolonged radiation on the diversity of heterotrophic bacteria in the soils of the 10-km zone around Chernobyl NPP. Mikrobio Zh Kiev 58:3–11
Sangali S, Brandelli A (2000) Feather keratin hydrolysis by a Vibrio sp. strain kr2. J Appl Microbiol 89:735–743
Shawkey MD, Mills KL, Dale C, Hill GE (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microb Ecol 50:40–47
Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349
Shawkey MD, Pillai SR, Hill GE (2009) Do feather-degrading bacteria affect sexually selected plumage color? Naturwissenschaften 96:123–128
Shestopalov VM (1996) Atlas of Chernobyl exclusion zone. Ukrainian Academy of Science, Kiev
Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2291
Vinogradov AE, Chubinishvili AT (1999) Genome reduction in a hemiclonal frog Rana esculanta from radioactively contaminated area. Genetics 151:1123–1125
Williams CM, Richter CS, MACKenzie JM Jr, Shih JCH (1990) Isolation, identification, and characterization of a feather-degrading bacterium. Appl Environ Microbiol 56:1509–1515
Yablokov AV, Nesterenko VB, Nesterenko AV (2009) Chernobyl: consequences of the catastrophe for people and nature. New York Academy of Sciences, New York
Zavilgelsky GB, Abilev SK, Sukhodolets VV, Ahmad SI (1998) Isolation and analysis of UV and radio-resistant bacteria from Chernobyl. J Photochem Photobiol B 43:152–157
Zhdanova NN, Zakharchenko VA, Vember VV, Nakonechnaya LT (2000) Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol Res 104:1421–1426
Acknowledgements
We are grateful to Emese and Sára Czirják, Mathieu Giraudeau, Alex R. Gunderson, Pascal Mirleau and Matthew D. Shawkey for their help. This project was supported in part by a French research grant from ANR to PH and Marcel Lambrechts (ANR-05, NT05-3_42075). GÁC was supported by a Ph.D. scholarship of the Romanian Ministry of Education and Research and by an Eiffel grant from the French Ministry of Foreign Affairs. APM and TAM gratefully acknowledge support from the CNRS (France), the US National Science Foundation, the National Geographic Society and the Samuel Freeman Charitable Trust. Three anonymous reviewers kindly provided constructive criticism on an earlier version of the manuscript.
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Czirják, G.Á., Møller, A.P., Mousseau, T.A. et al. Microorganisms Associated with Feathers of Barn Swallows in Radioactively Contaminated Areas Around Chernobyl. Microb Ecol 60, 373–380 (2010). https://doi.org/10.1007/s00248-010-9716-4
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DOI: https://doi.org/10.1007/s00248-010-9716-4