Abstract
Understanding linkages between biotic and abiotic processes operating in highly seasonal environments such as the Savannas in the Neotropics is tremendously challenging but has been aided considerably through biogeochemical markers. Stable isotope ratios have been widely used as spatial and temporal integrative markers, signaling environmental information. Our objective in this study was to examine the relationship of tissue δ18O and environmental factors and among multiple tissues in Saffron Finches, since this species is primary resident and abundant in the region. We conducted this study in a private farm in the central Brazilian savannas. We sampled 194 individuals in seven field samplings between January 2017 and March 2018. We collected whole blood, feathers and claws and analyzed them for δ18O in both the yellow (YEL) and dull (DULL) plumage categories. We built different sets of environmental variables as predictors of blood δ18O. Median blood δ18O varied widely throughout the year (13.4–18.8 ‰), differing in most pairwise comparison of months. Primary and tail feathers for both categories showed narrower isotopic median ranges compared to blood. Claw δ18O showed smaller isotopic ratio variation than the other tissues. Our results showed that δ18O values in avian blood are related to local climatic variables and reflect changes through time. The amount of precipitation, humidity and temperature were the most important environmental predictors. Therefore, the use of δ18O in different avian tissues could be used as a proxy to infer different environmental and ecological aspects related to the Saffron Finch.
Zusammenfassung
Umweltindikatoren und δ18O in Blut, Federn und Krallen der Safrangilbtangare ( Sicalis flaveola ) in den zentralbrasilianischen Savannen
Das Verständnis der Zusammenhänge zwischen biotischen und abiotischen Prozessen, die in stark saisonabhängigen Umgebungen wie den Savannen in der Neotropis ablaufen, ist eine enorme Herausforderung, die jedoch durch biogeochemische Marker erheblich erleichtert wurde. Stabile Isotopenverhältnisse werden häufig als räumliche und zeitliche integrative Marker verwendet, die Informationen über die Umwelt signalisieren. Unser Ziel in dieser Studie war es, die Beziehung zwischen Gewebe δ18O und Umweltfaktoren sowie zwischen verschiedenen Geweben bei Safrangilbtangaren zu untersuchen, da diese Art in der Region primär ansässig und häufig ist. Wir führten diese Studie auf einer privaten Farm in den zentralbrasilianischen Savannen durch. Zwischen Januar 2017 und März 2018 haben wir 194 Individuen in sieben Felduntersuchungen beprobt. Wir sammelten Vollblut, Federn und Krallen und analysierten sie auf δ18O sowohl in den gelben (YEL) als auch in den matten (DULL) Gefiederkategorien. Wir erstellten verschiedene Sätze von Umweltvariablen als Prädiktoren für δ18O im Blut. Der mittlere Blut-δ18O-Wert schwankte im Jahresverlauf stark (13,4 bis 18,8 ‰) und unterschied sich in den meisten paarweisen Vergleichen der Monate. Primär- und Schwanzfedern wiesen für beide Kategorien im Vergleich zum Blut engere isotopische Medianbereiche auf. Das δ18O der Krallen wies geringere Schwankungen im Isotopenverhältnis auf als die anderen Gewebe. Unsere Ergebnisse zeigen, dass die δ18O-Werte im Blut von Vögeln mit lokalen Klimavariablen zusammenhängen und Veränderungen im Laufe der Zeit widerspiegeln. Die Niederschlagsmenge, die Luftfeuchtigkeit und die Temperatur waren die wichtigsten Umweltprädiktoren. Daher könnte die Verwendung von δ18O in verschiedenen Vogelgeweben als Proxy verwendet werden, um verschiedene Umwelt- und ökologische Aspekte in Bezug auf die Safrangilbtangare abzuleiten.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abeni F, Petrera F, Capelletti M et al (2015) Hydrogen and oxygen stable isotope fractionation in body fluid compartments of dairy cattle according to season, farm, breed, and reproductive stage. PLoS ONE 10:e0127391. https://doi.org/10.1371/journal.pone.0127391
Aguilar TM, Dias RI, Oliveira AC et al (2008) Blue-black Grassquit nest-site selection in a Neotropical savanna: do choices influence nest success? J Field Ornithol 79:24–31
Alves RRN, De Farias Lima JR, Araujo HFP (2012) The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int. https://doi.org/10.1017/S095927091200010X
Anchukaitis KJ, Evans MN, Wheelwright NT et al (2008) Stable isotope chronology and climate signal calibration in neotropical montane cloud forest trees. J Geophys Res 113:3030. https://doi.org/10.1029/2007JG000613
Auerswald K, Rossmann A, Schäufele R et al (2011) Does natural weathering change the stable isotope composition (2H, 13C, 15N, 18O and 34S) of cattle hair? Rapid Commun Mass Spectrom 25(24):3741–3748
Baisden WT, Keller ED, Van Hale R et al (2016) Precipitation isoscapes for New Zealand: enhanced temporal detail using precipitation-weighted daily climatology. Isotopes Environ Health Stud 52:343–352. https://doi.org/10.1080/10256016.2016.1153472
Bearhop S, Furness RW, Hilton GM et al (2003) A Forensic Approach to Understanding Diet and Habitat Use from Stable Isotope Analysis of (Avian) Claw Material. Funct Ecol 17:270–275
Beuchle R, Grecchi RC, Shimabukuro YE et al (2015) Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Appl Geograph 58:116–127
Bontempo L, Ceppa F, Ziller L et al (2014) Comparison of methods for stable isotope ratio (δ13C, δ15N, δ2H, δ18O) measurements of feathers. Methods Ecol Evol 5(4):363–371
Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348. https://doi.org/10.1007/s00442-004-1813-y
Bowen GJ (2010) Statistical and geostatistical mapping of precipitation water isotope ratios. In: West JB, Bowen GJ, Dawson TE (eds) Isoscapes: spatial pattern in isotopic biogeochemistry. Annu Rev Earth Planet Sci, vol 38, pp 161–87. https://doi.org/10.1146/annurev-earth-040809-152429
Bryant JD, Froelich PN (1995) A model of oxygen isotope fractionation in body water of large mammals. Geochim Cosmochim Acta 59:4523–4537. https://doi.org/10.1016/0016-7037(95)00250-4
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoreticapproach. Springer, New York
Carter JF, Chesson LA (2017) Chapter 2: Sampling, sample preparation and analysis. In: Food Forensics. CRC Press, 6000 Broken Sound Parkway NW, Suite 300, Boca Raton, FL 33487–2742, pp 22–45
Cernusak LA, Barbour MM, Arndt SK et al (2016) Stable isotopes in leaf water of terrestrial plants. Plant Cell Environ 39:1087–1102. https://doi.org/10.1111/pce.12703
Chesson LA, Tipple BJ, Howa JD et al (2014) Stable isotopes in forensics applications. Treatise on Geochemistry. Elsevier, Amsterdam, pp 285–317
Clark I, Fritz P (1997) Environmental isotopes in hydrogeology. CRC Press, Taylor and Francis group, Boca Raton
Cordeiro GG (2019) Uso do δ13C como indicador da influência de pastagens cultivadas em zonas ripárias na bacia do Alto Corumbá. Dissertation, Universidade de Brasília
Costa FJV, Ribeiro RE, De Souza CA et al (2018) Espécies de Aves Traficadas no Brasil. Front J Soc Technol Environ Sci 7:324–346. https://doi.org/10.21664/2238-8869.2018v7i2
Cryan PM, Stricker CA, Wunder MB (2014) Continental-scale, seasonal movements of a heterothermic migratory tree bat. Ecol Appl 24:602–616. https://doi.org/10.1890/13-0752.1
Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468. https://doi.org/10.3402/tellusa.v16i4.8993
Dawson TE, Siegwolf RTW (2007) Stable isotopes as indicators of ecological change. Academic press, London
Paiva LV De (2008) Fatores que determinam o período reprodutivo de Elaenia chiriquensis (Aves: Tyrannidae) no cerrado do Brasil central. Dissertation, Universidade de Brasília
Destro GFG, Lucena T, Monti R et al (2012) Efforts to combat wild animals trafficking in Brazil. Biodivers Enrich a Divers World 1542:33–36. https://doi.org/10.5772/48351
Ehleringer JR, Bowen GJ, Chesson LA et al (2008) Hydrogen and oxygen isotope ratios in human hair are related to geography. Proc Natl Acad Sci 105:2788–2793. https://doi.org/10.1073/pnas.0712228105
Flockhart DTT, Wassenaar LI, Martin TG et al (2013) Tracking multi-generational colonization of the breeding grounds by monarch butterflies in eastern North America. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2013.1087
Francisco MR (2006) Breeding biology of the double-collared Seedeater (Sporophila caerulescens). Wilson J Ornithol 118:85–90
Garcia-Perez B, Hobson KA, Powell RL et al (2013) Switching hemispheres: a new migration strategy for the Disjunct Argentinean breeding population of Barn Swallow (Hirundo rustica). PLoS ONE 8:e55654. https://doi.org/10.1371/journal.pone.0055654
García-Pérez B, Hobson K (2014) A multi-isotope (δ2H, δ13C, δ15N) approach to establishing migratory connectivity of Barn Swallow (Hirundo rustica). Ecosphere 5:1–12. https://doi.org/10.3161/000164514X682896
Gat JR, Klein B, Kushnir Y et al (2011) Isotope composition of air moisture over the Mediterranean Sea: an index of the air-sea interaction pattern. Tellus B Chem Phys Meteorol 55(5):953–965. https://doi.org/10.3402/tellusb.v55i5.16395
Giustini F, Brilli M, Patera A (2016) Mapping oxygen stable isotopes of precipitation in Italy. J Hydrol. https://doi.org/10.1016/j.ejrh.2016.04.001
Gressler DT, Marini MÂ (2011) Breeding biology of the Stripe-tailed Yellow-Finch (Sicalis citrina) in central Brazilian cerrado. Ornitol Neotropical 22:319–328
Hobson KA, Koehler G (2015) On the use of stable oxygen isotope (δ 18O) measurements for tracking avian movements in North America. Ecol Evol 5:799–806. https://doi.org/10.1002/ece3.1383
Hobson KA, Wassenaar LI (2019) Tracking animal migration with stable isotopes, 2nd. Academic Press, New York
Hobson KA, Van Wilgenburg SL, Faaborg J et al (2014) Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity. J Field Ornithol 85:237–257
Hunke P, Mueller EM, Schroder B et al (2015) The Brazilian Cerrado: assessment of water and soil degradation in catchments under intensive agricultural use. Ecohydrology 8:1154–1180
Koehler G, Hobson KA (2019) Tracking cats revisited: placing terrestrial mammalian carnivores on δ2H and δ18O isoscapes. PLoS ONE 4(9):e0221876. https://doi.org/10.1371/journal.pone.0221876
Magozzi S, Vander Zanden HB, Wunder MB et al (2019) Mechanistic model predicts tissue–environment relationships and trophic shifts in animal hydrogen and oxygen isotope ratios. Oecologia 191:777–789. https://doi.org/10.1007/s00442-019-04532-8
Marcondes-Machado LO (2002) Canário-da-terra (Sicalis flaveola) Comportamento reprodutivo e social Repovoamento, 1st edn. Santa Edwiges, São Paulo
Marini MÂ, Barbet-Massin M, Lopes LE et al (2009) Predicted climate-driven bird distribution changes and forecasted conservation conflicts in a neotropical savanna. Conserv Biol 23:1558–1567. https://doi.org/10.1111/j.1523-1739.2009.01258.x
Marini MÂ, Borges FJA, Lopes LE et al (2012) Breeding biology of birds in the Cerrado. Ornitol Neotropical 23:385–405
Marques-Santos F, Wischhoff U, Roper JJ et al (2018) Delayed plumage maturation explains differences in breeding performance of Saffron Finches. Emu 118:323–333. https://doi.org/10.1080/01584197.2018.1450637
Meier-Augenstein W, Fraser I (2008) Forensic isotope analysis leads to identification of a mutilated murder victim. Sci Justice 48:153–159. https://doi.org/10.1016/j.scijus.2007.10.010
Mittermeier RA, Turner WR, Larsen FW et al (2011) Global biodiversity conservation: the critical role of hotspots. In: Biodiversity Hotspots, pp 3–22
Instituto Nacional de Meteorologia (2019) Banco de Dados Meteorológicos para Ensino e Pesquisa—Dados historicos. http://www.inmet.gov.br. Acessed 15 Apr 2019
Palmerio AG, Massoni V (2009) Reproductive biology of female Saffron Finches does not Differ by the Plumage of the Mate. Condor 111:715–721. https://doi.org/10.1525/cond.2009.080044
Piacentini VQ, Aleixo A, Agne CE et al (2015) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee/Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Rev Bras Ornitol 23:91–298
Pietsch SJ, Hobson KA, Wassenaar LI, Tü Tken T (2011) Tracking Cats: problems with placing Feline Carnivores on δ18O, D Isoscapes. PLoS ONE. https://doi.org/10.1371/journal.pone.0024601
Pinto JRR, Lenza E, Pinto AS (2009) Composição florística e estrutura da vegetação arbustivo-arbórea em um cerrado rupestre, Cocalzinho de Goiás, Goiás. Rev Bras Bot 32:1–10. https://doi.org/10.1590/s0100-84042009000100002
Quillfeldt P, Bugoni L, McGill RAR et al (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598. https://doi.org/10.1007/s00227-008-1048-2
Remsen JV Jr, Areta JI, Bonaccorso E et al (2016) A classification of the bird species of South America. American Ornithologists’ Union. South Am Classif Commun. http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm. Accessed 23 Dec 2016
Rising J, Jaramillo A (2017) Saffron Finch (Sicalis flaveola). In: del Hoyo J, Elliott A, Sargatal J, et al (eds) Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. (retrieved from http://www.hbw.com/node/62084. Accessed 18 Jul 2017
Silveira MB, Marini MA (2012) Timing, duration, and intensity of Molt in Birds of a Neotropical Savanna in Brazil. Condor 114:435–448. https://doi.org/10.1525/cond.2012.110022
Soto DX, Wassenaar LI, Hobson KA (2013) Stable hydrogen and oxygen isotopes in aquatic food webs are tracers of diet and provenance. Funct Ecol 27:535–543. https://doi.org/10.1111/1365-2435.12054
Terzer S, Wassenaar LI, Araguás-Araguás LJ et al (2013) Global isoscapes for δ18O and δ2H in precipitation: improved prediction using regionalized climatic regression models. Hydrol Earth Syst Sci 17:4713–4728. https://doi.org/10.5194/hess-17-4713-2013
Vander Zanden HB, Tucker AD, Bolten AB et al (2014) Stable isotopic comparison between loggerhead sea turtle tissues. Rapid Commun Mass Spectrom 28(19):2059–2064
Vander Zanden MJ, Clayton MK, Moody EK et al (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS ONE 10(1):e0116182
Vander Zanden HB, Soto DX, Bowen GJ et al (2016) Expanding the isotopic toolbox: applications of hydrogen and oxygen stable isotope ratios to food web studies. Front Ecol Evol 4:20. https://doi.org/10.3389/fevo.2016.00020
Vander Zanden HB, Nelson DM, Wunder MB et al (2018) Application of isoscapes to determine geographic origin of terrestrial wildlife for conservation and management. Biol Conserv 228:268–280
Voigt CC, Schneeberger K, Luckner A (2013) Ecological and dietary correlates of stable hydrogen isotope ratios in fur and body water of syntopic tropical bats. Ecology 94:346–355. https://doi.org/10.2307/23435982
Wassenaar LI (2019) Introduction to conducting stable isotope measurements for animal migration studies. In: Hobson KA, Wassenaar LI (eds) Introduction to conducting stable isotope measurements for animal migration studies, 2nd edn. Academic Press, New York, pp 25–51
Wassenaar LI, Hobson KA (1998) Natal origins of migratory monarch butterflies at wintering colonies in Mexico: New isotopic evidence. Proc Natl Acad Sci 95:15436–15439. https://doi.org/10.1073/pnas.95.26.15436
West JB, Bowen GJ, Dawson TE, Tu KP (2010) Isoscapes: understanding movement, pattern, and process on easrth through isotope mapping. Springer, Dordrecht, Heidelberg, London
Wolf N, Bowen GJ, del Rio CM (2011) The influence of drinking water on the δ2H and δ18O values of house sparrow plasma, blood and feathers. J Exp Biol 214:98–103. https://doi.org/10.1242/jeb.050211
Zazzo A, Cerling TE, Ehleringer JR et al (2015) Isotopic composition of sheep wool records seasonality of climate and diet. Rapid Commun Mass Spectrom 29:1357–1369. https://doi.org/10.1002/rcm.7228
Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
We are thankful to the Tabapuã do Pireneus farm and workers who helped with the field work. We thank the Environmental Isotope Studies–University of Brasília group for all the scientific discussion and help in the field. We also thank to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001 and Edital Capes Pro-Forense/2014 (grant number 23038.006832/2014-11) which financed this study.
Author information
Authors and Affiliations
Contributions
FJVC and GBN contributed to the study conception and design. Material preparation and data collection were performed by FJVC. KAH and MBW contributed to the data interpretation, statistical analysis and manuscript outline and writing. The first draft of the manuscript was written by FJVC and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Additional information
Communicated by C. G. Guglielmo.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Costa, F.J.V., Hobson, K.A., Wunder, M.B. et al. Linking environmental indicators to blood, feather and claw δ18O in the Saffron Finch (Sicalis flaveola) in the central Brazilian savannas. J Ornithol 163, 223–234 (2022). https://doi.org/10.1007/s10336-021-01939-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-021-01939-0