Plumage iridescence is associated with distinct feather microbiota in a tropical passerine

. 2019 Sep 09 ; 9 (1) : 12921. [epub] 20190909

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid31501471
Odkazy

PubMed 31501471
PubMed Central PMC6733896
DOI 10.1038/s41598-019-49220-y
PII: 10.1038/s41598-019-49220-y
Knihovny.cz E-zdroje

Birds present a stunning diversity of plumage colors that have long fascinated evolutionary ecologists. Although plumage coloration is often linked to sexual selection, it may impact a number of physiological processes, including microbial resistance. At present, the degree to which differences between pigment-based vs. structural plumage coloration may affect the feather microbiota remains unanswered. Using quantitative PCR and DGGE profiling, we investigated feather microbial load, diversity and community structure among two allopatric subspecies of White-shouldered Fairywren, Malurus alboscapulatus that vary in expression of melanin-based vs. structural plumage coloration. We found that microbial load tended to be lower and feather microbial diversity was significantly higher in the plumage of black iridescent males, compared to black matte females and brown individuals. Moreover, black iridescent males had distinct feather microbial communities compared to black matte females and brown individuals. We suggest that distinctive nanostructure properties of iridescent male feathers or different investment in preening influence feather microbiota community composition and load. This study is the first to point to structural plumage coloration as a factor that may significantly regulate feather microbiota. Future work might explore fitness consequences and the role of microorganisms in the evolution of avian sexual dichromatism, with particular reference to iridescence.

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Echeverry-Galvis Maria Angela, Hau Michaela. Flight Performance and Feather Quality: Paying the Price of Overlapping Moult and Breeding in a Tropical Highland Bird. PLoS ONE. 2013;8(5):e61106. doi: 10.1371/journal.pone.0061106. PubMed DOI PMC

Tomotani BM, Muijres FT, Koelman J, Casagrande S, Visser ME. Simulated moult reduces flight performance but overlap with breeding does not affect breeding success in a long-distance migrant. Funct. Ecol. 2018;32:389–401. doi: 10.1111/1365-2435.12974. DOI

Pap PL, et al. Interspecific variation in the structural properties of flight feathers in birds indicates adaptation to flight requirements and habitat. Funct. Ecol. 2015;29:746–757. doi: 10.1111/1365-2435.12419. DOI

Osvath G, et al. How feathered are birds? Environment predicts both the mass and density of body feathers. Funct. Ecol. 2018;32:701–712. doi: 10.1111/1365-2435.13019. DOI

Butler LK, Rohwer S, Speidel MG. Quantifying structural variation in contour feathers to address functional variation and life history trade-offs. J. Avian Biol. 2008;39:629–639. doi: 10.1111/j.1600-048X.2008.04432.x. DOI

Pap PL, et al. A phylogenetic comparative analysis reveals correlations between body feather structure and habitat. Funct. Ecol. 2017;31:1241–1251. doi: 10.1111/1365-2435.12820. DOI

Penteriani Vincenzo, Delgado María del Mar. Living in the dark does not mean a blind life: bird and mammal visual communication in dim light. Philosophical Transactions of the Royal Society B: Biological Sciences. 2017;372(1717):20160064. doi: 10.1098/rstb.2016.0064. PubMed DOI PMC

Moller AP, Cuervo JJ. Speciation and feather ornamentation in birds. Evolution. 1998;52:859–869. doi: 10.2307/2411280. PubMed DOI

Galván Ismael, Solano Francisco. Bird Integumentary Melanins: Biosynthesis, Forms, Function and Evolution. International Journal of Molecular Sciences. 2016;17(4):520. doi: 10.3390/ijms17040520. PubMed DOI PMC

LaFountain AM, Prum RO, Frank HA. Diversity, physiology, and evolution of avian plumage carotenoids and the role of carotenoid-protein interactions in plumage color appearance. Arch. Biochem. Biophys. 2015;572:201–212. doi: 10.1016/j.abb.2015.01.016. PubMed DOI

Igic B, D’Alba L, Shawkey MD. Manakins can produce iridescent and bright feather colours without melanosomes. J. Exp. Biol. 2016;219:1851–1859. doi: 10.1242/jeb.137182. PubMed DOI

Doucet SM, Shawkey MD, Hill GE, Montgomerie R. Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour. J. Exp. Biol. 2006;209:380–390. doi: 10.1242/jeb.01988. PubMed DOI

Shawkey MD, D’Alba L. Interactions between colour-producing mechanisms and their effects on the integumentary colour palette. Philos. T. R. Soc. B. 2017;372:9. doi: 10.1098/rstb.2016.0536. PubMed DOI PMC

D’Alba L, et al. Melanin-Based Color of Plumage: Role of Condition and of Feathers’ Microstructure. Integr. Comp. Biol. 2014;54:633–644. doi: 10.1093/icb/icu094. PubMed DOI

Eliason Chad M., Bitton Pierre-Paul, Shawkey Matthew D. How hollow melanosomes affect iridescent colour production in birds. Proceedings of the Royal Society B: Biological Sciences. 2013;280(1767):20131505. doi: 10.1098/rspb.2013.1505. PubMed DOI PMC

Dakin R, Montgomerie R. Eye for an eyespot: how iridescent plumage ocelli influence peacock mating success. Behav. Ecol. 2013;24:1048–1057. doi: 10.1093/beheco/art045. DOI

Maia R, Caetano JVO, Bao SN, Macedo RH. Iridescent structural colour production in male blue-black grassquit feather barbules: the role of keratin and melanin. J. R. Soc. Interface. 2009;6:S203–S211. doi: 10.1098/rsif.2008.0460.focus. PubMed DOI PMC

Hill, G. E. & McGraw, K. J. Bird Coloration, Volume 2: Function and Evolution. (Harvard University Press, 2006).

Van Wijk S, Bourret A, Belisle M, Garant D, Pelletier F. The influence of iridescent coloration directionality on male tree swallows’ reproductive success at different breeding densities. Behav. Ecol. Sociobiol. 2016;70:1557–1569. doi: 10.1007/s00265-016-2164-5. DOI

Owens IPF, Hartley IR. Sexual dimorphism in birds: why are there so many different forms of dimorphism? P. R. Soc. B. 1998;265:397–407. doi: 10.1098/rspb.1998.0308. DOI

Garratt M, Brooks RC. Oxidative stress and condition-dependent sexual signals: more than just seeing red. P. R. Soc. B. 2012;279:3121–3130. doi: 10.1098/rspb.2012.0568. PubMed DOI PMC

Loyau A, et al. Iridescent structurally based coloration of eyespots correlates with mating success in the peacock. Behav. Ecol. 2007;18:1123–1131. doi: 10.1093/beheco/arm088. DOI

Price TD. Phenotypic plasticity, sexual selection and the evolution of colour patterns. J. Exp. Biol. 2006;209:2368–2376. doi: 10.1242/jeb.02183. PubMed DOI

Badyaev AV, Hill GE. Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol. J. Linn. Soc. 2000;69:153–172. doi: 10.1111/j.1095-8312.2000.tb01196.x. DOI

Thompson CW, Hillgarth N, Leu M, McClure HE. High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am. Nat. 1997;149:270–294. doi: 10.1086/285990. DOI

Meunier J, Pinto SF, Burri R, Roulin A. Eumelanin-based coloration and fitness parameters in birds: a meta-analysis. Behav. Ecol. Sociobiol. 2011;65:559–567. doi: 10.1007/s00265-010-1092-z. DOI

Roulin A. Condition-dependence, pleiotropy and the handicap principle of sexual selection in melanin-based colouration. Biol. Rev. 2016;91:328–348. doi: 10.1111/brv.12171. PubMed DOI

Shawkey MD, Mills KL, Dale C, Hill GE. Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microb. Ecol. 2005;50:40–47. doi: 10.1007/s00248-004-0089-4. PubMed DOI

Kent CM, Burtt EH. Feather-degrading bacilli in the plumage of wild birds: Prevalence and relation to feather wear. Auk. 2016;133:583–592. doi: 10.1642/auk-16-39.1. DOI

Bisson IA, Marra PP, Burtt EH, Sikaroodi M, Gillevet PM. Variation in Plumage Microbiota Depends on Season and Migration. Microb. Ecol. 2009;58:212–220. doi: 10.1007/s00248-009-9490-3. PubMed DOI

Javůrková Veronika Gvoždíková, Kreisinger Jakub, Procházka Petr, Požgayová Milica, Ševčíková Kateřina, Brlík Vojtěch, Adamík Peter, Heneberg Petr, Porkert Jiří. Unveiled feather microcosm: feather microbiota of passerine birds is closely associated with host species identity and bacteriocin-producing bacteria. The ISME Journal. 2019;13(9):2363–2376. doi: 10.1038/s41396-019-0438-4. PubMed DOI PMC

Miskiewicz A, Kowalczyk P, Oraibi SM, Cybulska K, Misiewicz A. Bird feathers as potential sources of pathogenic microorganisms: a new look at old diseases. Anton. Leeuw. Int. J. G. 2018;111:1493–1507. doi: 10.1007/s10482-018-1048-2. PubMed DOI PMC

Gunderson AR. Feather-degrading bacteria: a new frontier in avian and host-parasite research? Auk. 2008;125:972–979. doi: 10.1525/auk.2008.91008. DOI

Goldstein G, et al. Bacterial degradation of black and white feathers. Auk. 2004;121:656–659. doi: 10.1642/0004-8038. DOI

Gunderson AR, Frame AM, Swaddle JP, Forsyth MH. Resistance of melanized feathers to bacterial degradation: is it really so black and white? J. Avian Biol. 2008;39:539–545. doi: 10.1111/j.2008.0908-8857.04413.x. DOI

Shawkey MD, Pillai SR, Hill GE, Siefferman LM, Roberts SR. Bacteria as an agent for change in structural plumage color: Correlational and experimental evidence. Am. Nat. 2007;169:S112–S121. doi: 10.1086/510100. PubMed DOI

Shawkey MD, Pillai SR, Hill GE. Do feather-degrading bacteria affect sexually selected plumage color? Naturwissenschaften. 2009;96:123–128. doi: 10.1007/s00114-008-0462-0. PubMed DOI

Leclaire S, Pierret P, Chatelain M, Gasparini J. Feather bacterial load affects plumage condition, iridescent color, and investment in preening in pigeons. Behav. Ecol. 2014;25:1192–1198. doi: 10.1093/beheco/aru109. DOI

Leclaire S, Czirjak GA, Hammouda A, Gasparini J. Feather bacterial load shapes the trade-off between preening and immunity in pigeons. BMC Evol. Biol. 2015;15:8. doi: 10.1186/s12862-015-0338-9. PubMed DOI PMC

Saag P, et al. Plumage bacterial load is related to species, sex, biometrics and fledging success in co-occurring cavity-breeding passerines. Acta Ornithol. 2011;46:191–201. doi: 10.3161/000164511x62596. DOI

Horrocks Nicholas P. C., Matson Kevin D., Shobrak Mohammed, Tinbergen Joost M., Tieleman B. Irene. Seasonal patterns in immune indices reflect microbial loads on birds but not microbes in the wider environment. Ecosphere. 2012;3(2):art19. doi: 10.1890/ES11-00287.1. DOI

Burtt EH, Schroeder MR, Smith LA, Sroka JE, McGraw KJ. Colourful parrot feathers resist bacterial degradation. Biol. Lett. 2011;7:214–216. doi: 10.1098/rsbl.2010.0716. PubMed DOI PMC

Ruiz-De-Castaneda R, Burtt EH, Gonzalez-Braojos S, Moreno J. Bacterial degradability of an intrafeather unmelanized ornament: a role for feather-degrading bacteria in sexual selection? Biol.J. Linn. Soc. 2012;105:409–419. doi: 10.1111/j.1095-8312.2011.01806.x. DOI

Justyn NM, Peteya JA, D’Alba L, Shawkey MD. Preferential attachment and colonization of the keratinolytic bacterium Bacillus licheniformis on black- and white-striped feathers. Auk. 2017;134:466–473. doi: 10.1642/auk-16-245.1. DOI

Galeotti P, Rubolini D, Dunn PO, Fasola M. Colour polymorphism in birds: causes and functions. J. Evol. Biol. 2003;16:635–646. doi: 10.1046/j.1420-9101.2003.00569.x. PubMed DOI

Delhey K. Darker where cold and wet: Australian birds follow their own version of Gloger’s rule. Ecography. 2018;41:673–683. doi: 10.1111/ecog.03040. DOI

Zink, R. M. & Remsen, J. V. J. Evolutionary processes and patterns of geographic variation in birds., Vol. 4 1–69 (Plenum Press, 1986).

Burtt EH, Ichida JM. Gloger’s rule, feather-degradlng bacteria, and color variation among song sparrows. Condor. 2004;106:681–686. doi: 10.1650/7383. DOI

Maia R, Rubenstein DR, Shawkey MD. Selection, constraint, and the evolution of coloration in African starlings. Evolution. 2016;70:1064–1079. doi: 10.1111/evo.12912. PubMed DOI

Eliason CM, Maia R, Shawkey MD. Modular color evolution facilitated by a complex nanostructure in birds. Evolution. 2015;69:357–367. doi: 10.1111/evo.12575. PubMed DOI

Hung, H. Y. et al. Himalayan black bulbuls (Hypsipetes leucocephalus niggerimus) exhibit sexual dichromatism under ultraviolet light that is invisible to the human eye. Sci. Rep. 7, 10.1038/srep43707 (2017). PubMed PMC

Hu, D. Y. et al. A bony-crested Jurassic dinosaur with evidence of iridescent plumage highlights complexity in early paravian evolution. Nat. Comm. 9, 10.1038/s41467-017-02515-y (2018). PubMed PMC

Eliason CM, Shawkey MD. Decreased hydrophobicity of iridescent feathers: a potential cost of shiny plumage. J. Exp. Biol. 2011;214:2157–2163. doi: 10.1242/jeb.055822. PubMed DOI

Ruiz-Rodriguez M, Tomas G, Martin-Galvez D, Ruiz-Castellano C, Soler JJ. Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings. Funct. Ecol. 2015;29:701–709. doi: 10.1111/1365-2435.12376. DOI

Simpson RK, McGraw KJ. Two ways to display: male hummingbirds show different color-display tactics based on sun orientation. Behav. Ecol. 2018;29:637–648. doi: 10.1093/beheco/ary016. DOI

Taysom AJ, Stuart-Fox D, Cardoso GC. The contribution of structural-, psittacofulvin- and melanin-based colouration to sexual dichromatism in Australasian parrots. J. Evol. Biol. 2011;24:303–313. doi: 10.1111/j.1420-9101.2010.02166.x. PubMed DOI

Doucet SM, Montgomerie R. Structural plumage colour and parasites in satin bowerbirds Ptilonorhynchus violaceus: implications for sexual selection. J. Avian Biol. 2003;34:237–242. doi: 10.1034/j.1600-048X.2003.03113.x. DOI

Doucet SM, Meadows MG. Iridescence: a functional perspective. J. R. Soc. Interface. 2009;6:S115–S132. doi: 10.1098/rsif.2008.0395.focus. PubMed DOI PMC

Bisson IA, Marra PP, Burtt EH, Sikaroodi M, Gillevet PM. A molecular comparison of plumage and soil bacteria across biogeographic, ecological, and taxonomic scales. Microb. Ecol. 2007;54:65–81. doi: 10.1007/s00248-006-9173-2. PubMed DOI

Pajares, S., Bohannan, B. J. M. & Souza, V. Editorial: The Role of Microbial Communities in Tropical Ecosystems. Front. Microbiol. 7, 10.3389/fmicb.2016.01805 (2016). PubMed PMC

Bush Sarah E., Clayton Dale H. Anti-parasite behaviour of birds. Philosophical Transactions of the Royal Society B: Biological Sciences. 2018;373(1751):20170196. doi: 10.1098/rstb.2017.0196. PubMed DOI PMC

Rowley, I. & Russell, E. Fairy-wrens and Grasswrens: Maluridae., (Oxford: Oxforfd University Press, 1997).

Enbody ED, et al. Social organisation and breeding biology of the White-shouldered Fairywren (Malurus alboscapulatus) Emu. 2019;119:274–285. doi: 10.1080/01584197.2019.1595663. DOI

Enbody ED, Lantz SM, Karubian J. Production of plumage ornaments among males and females of two closely related tropical passerine bird species. Ecol. Evol. 2017;7:4024–4034. doi: 10.1002/ece3.3000. PubMed DOI PMC

Fridolfsson AK, Ellegren H. A simple and universal method for molecular sexing of non-ratite birds. Journal of Avian Biology. 1999;30:116–121. doi: 10.2307/3677252. DOI

Kahn NW, St John J, Quinn TW. Chromosome-specific intron size differences in the avian CHD gene provide an efficient method for sex identification in birds. Auk. 1998;115:1074–1078. doi: 10.2307/4089527. DOI

McMurdie PJ, Holmes S. phyloseq:an Rpackage for reproducible interactive analysis and graphics o microbiome census data. PLoS ONE. 2013;8:e61217. doi: 10.1371/journal.pone.0061217. PubMed DOI PMC

Muyzer G, Dewaal EC, Uitterlinden AG. Profiling of complex microbial-populations by Denaturing Gradient Gel-Electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA. Appl.Environ. Microbiol. 1993;59:695–700. PubMed PMC

Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ.Microbiol. 2007;73:5261–5267. doi: 10.1128/aem.00062-07. PubMed DOI PMC

DeSantis TZ, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ.Microbiol. 2006;72:5069–5072. doi: 10.1128/aem.03006-05. PubMed DOI PMC

Yu G, Lam TTY, Zhu H, Guan Y. Two methods for mapping and visualizing associated data on phylogeny using ggtree. Mol. Biol. Evol. 2018;35(2):3041–3043. doi: 10.1093/molbev/msy194. PubMed DOI PMC

Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2018;35:526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI

Wickham, H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York, USA (2016).

RStudio Team RStudio: Integrated Development for R. RStudio, Inc., Boston, MA URL, http://www.rstudio.com/ (2015).

Anderson MJ, Walsh DC. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol. monogr. 2013;83:557–574. doi: 10.1890/12-2010.1. DOI

van Veelen, H. P. J., Salles, J. F. & Tieleman, B. I. Multi-level comparisons of cloacal, skin, feather and nest-associated microbiota suggest considerable influence of horizontal acquisition on the microbiota assembly of sympatric woodlarks and skylarks. Microbiome5, 10.1186/s40168-017-0371-6 (2017). PubMed PMC

Jacob S, et al. Chemical regulation of body feather microbiota in a wild bird. Mol. Ecol. 2018;27:1727–1738. doi: 10.1111/mec.14551. PubMed DOI

Jacob J, Eigener U, Hoppe U. The structure of preen gland waxes from pelecaniform birds containing 3,7-dimethyloctan-1-ol - An active ingredient against dermatophytes. Z. Naturforsch. C. 1997;52:114–123. doi: 10.1515/znc-1997-1-220. DOI

Shawkey MD, Pillai SR, Hill GE. Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J. Avian Biol. 2003;34:345–349. doi: 10.1111/j.0908-8857.2003.03193.x. DOI

Peralta-Sanchez JM, Moller AP, Martin-Platero AM, Soler JJ. Number and colour composition of nest lining feathers predict eggshell bacterial community in barn swallow nests: an experimental study. Funct. Ecol. 2010;24:426–433. doi: 10.1111/j.1365-2435.2009.01669.x. DOI

Roulin A. Melanin pigmentation negatively correlates with plumage preening effort in barn owls. Funct. Ecol. 2007;21:264–271. doi: 10.1111/j.1365-2435.2006.01229.x. DOI

Czirjak GA, et al. Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria. Naturwissenschaften. 2013;100:145–151. doi: 10.1007/s00114-012-1005-2. PubMed DOI

Giraudeau M, et al. Effects of access to preen gland secretions on mallard plumage. Naturwissenschaften. 2010;97:577–581. doi: 10.1007/s00114-010-0673-z. PubMed DOI

Griggio M, Hoi H, Pilastro A. Plumage maintenance affects ultraviolet colour and female preference in the budgerigar. Behav. Proc. 2010;84:739–744. doi: 10.1016/j.beproc.2010.05.003. PubMed DOI

Lopez-Rull I, Pagan I, Garcia CM. Cosmetic enhancement of signal coloration: experimental evidence in the house finch. Behav. Ecol. 2010;21:781–787. doi: 10.1093/beheco/arq053. DOI

Giraudeau M, Stikeleather R, McKenna J, Hutton P, McGraw KJ. Plumage micro-organisms and preen gland size in an urbanizing context. Sci. Total Environ. 2017;580:425–429. doi: 10.1016/j.scitotenv.2016.09.224. PubMed DOI

Fulop A, Czirjak GA, Pap PL, Vagasi CI. Feather-degrading bacteria, uropygial gland size and feather quality in House Sparrows Passer domesticus. Ibis. 2016;158:362–370. doi: 10.1111/ibi.12342. DOI

Jacob Staffan, Immer Anika, Leclaire Sarah, Parthuisot Nathalie, Ducamp Christine, Espinasse Gilles, Heeb Philipp. Uropygial gland size and composition varies according to experimentally modified microbiome in Great tits. BMC Evolutionary Biology. 2014;14(1):134. doi: 10.1186/1471-2148-14-134. PubMed DOI PMC

Walther BA, Clayton DH. Elaborate ornaments are costly to maintain: evidence for high maintenance handicaps. Behav. Ecol. 2005;16:89–95. doi: 10.1093/beheco/arh135. DOI

Viblanc Vincent A., Mathien Adeline, Saraux Claire, Viera Vanessa M., Groscolas René. It Costs to Be Clean and Fit: Energetics of Comfort Behavior in Breeding-Fasting Penguins. PLoS ONE. 2011;6(7):e21110. doi: 10.1371/journal.pone.0021110. PubMed DOI PMC

Pérez-Rodríguez Lorenzo, Jovani Roger, Stevens Martin. Shape matters: animal colour patterns as signals of individual quality. Proceedings of the Royal Society B: Biological Sciences. 2017;284(1849):20162446. doi: 10.1098/rspb.2016.2446. PubMed DOI PMC

Shawkey MD, et al. Beyond colour: consistent variation in near infrared and solar reflectivity in sunbirds (Nectariniidae) Sci. Nat-Heidelberg. 2017;104:5. doi: 10.1007/s00114-017-1499-8. PubMed DOI

McGraw KJ. Multiple UV reflectance peaks in the iridescent neck feathers of pigeons. Naturwissenschaften. 2004;91:125–129. doi: 10.1007/s00114-003-0498-0. PubMed DOI

Kinoshita S, Yoshioka S, Miyazaki J. Physics of structural colors. Reports on Progress in Physics. 2008;71(7):076401. doi: 10.1088/0034-4885/71/7/076401. DOI

Nelson KL, et al. Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches. Environ. Sci.-Proc. Imp. 2018;20:1089–1122. doi: 10.1039/c8em00047f. PubMed DOI PMC

Probst-Rud S, McNeill K, Ackermann M. Thiouridine residues in tRNAs are responsible for a synergistic effect of UVA and UVB light in photoinactivation of Escherichia coli. Environ. Microbiol. 2017;19:434–442. doi: 10.1111/1462-2920.13319. PubMed DOI

Zepp RG, Callaghan TV, Erickson DJ. Effects of enhanced solar ultraviolet radiation on biogeochemical cycles. J. Photoch.Photobio. B. 1998;46:69–82. doi: 10.1016/s1011-1344(98)00186-9. DOI

Doña J, et al. Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy. Mol. Ecol. 2019;28:203–218. doi: 10.1111/mec.14581. PubMed DOI PMC

Doña J, Proctor H, Mironov S, Serrano D, Jovani R. Global associations between birds and vane‐dwelling feather mites. Ecology. 2016;97:3242–3242. doi: 10.1002/ecy.1528. PubMed DOI

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