Perspectives and challenges on isotopic ecology of terrestrial birds in Brazil

Ana Beatriz Navarro Marcelo Magioli Marcelo Zacharias Moreira Luís Fábio Silveira About the authors

ABSTRACT

Although stable isotopes have been increasingly used in ornithology since 1980 in many places, Brazil has been slow in adopting this methodology, especially when it comes to terrestrial birds. The most common elements in bird ecology studies are carbon, nitrogen, hydrogen, and oxygen stable isotopes, which provide information on diet, trophic interactions, habitat use, migration, geographic patterns, and physiology. It is important that Brazilian ornithologists become aware of the potential of stable isotope analysis in ecological studies, and the shortcomings of this tool. The use of stable isotopes to study bird ecology has great potential in Brazil, since many ecological questions about Neotropical birds can be addressed by it (e.g., resource and habitat use, migratory routes, isotopic niches, anthropogenic impacts, individual specialization). Brazilian museums and other Natural History collections can provide samples to study long-term temporal dynamics in bird ecology. Additionally, the integration of avian tissue sample information into a database may increase the collaboration among researchers and promote sample reuse in a variety of studies. All biomes in Brazil have been under pressure from anthropogenic impacts (e.g., land-use change, habitat loss, fragmentation, intensive agriculture), affecting several taxa, including terrestrial birds. Considering the negative effects of human expansion over natural areas and that stable isotopes provide useful ecological information, ornithologists in Brazil should increase their use of this tool in the future.

KEY WORDS:
δ13C; δ15N; δ2H; δ18O; migratory birds; museum specimens; ornithology; trophic ecology

The isotopic methodology generates ornithological information that used to be only possible with conventional approaches (e.g., regurgitates or stomach contents analyses, tracking with GPS and telemetry, bird ringing). Using a single sample that can be collected through a minimally invasive method, stable isotopes make it possible to gather long-term information about organisms (Newton 2016Newton J (2016) Stable Isotopes as Tools inEcological Research. In: eLS Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, 1-8. https://doi.org/10.1002/9780470015902.a0021231.pub2
https://doi.org/10.1002/9780470015902.a0...
). Despite the advantages of this method, it has not been consistently employed in ornithological studies in Brazil. Brazilian studies are generally based on time-consuming and resource-demanding traditional methods that only offer a ‘snapshot’ of the diet of a bird.

Stable isotope analysis in ornithological studies is relatively recent worldwide, since the first studies were published in the 1980s (Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
). In Brazil, this methodology was first employed less than 20 years ago (Atkinson et al. 2005Atkinson PW, Baker AJ, Bevan RM, Clark NA, Cole KB, Gonzalez PM, Newton J, Niles LJ, Robinson RA (2005) Unravelling the migration and moult strategies of a long-distance migrant using stable isotopes: Red Knot Calidris canutus movements in the Americas. Ibis 147(4): 738-749. https://doi.org/10.1111/j.1474-919x.2005.00455.x
https://doi.org/10.1111/j.1474-919x.2005...
, Quillfeldt et al. 2008Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Marine Biology 155: 593-598., Bugoni et al. 2008Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Communications in Mass Spectrometry 22(16): 2457-2462. https://doi.org/10.1002/rcm.3633
https://doi.org/10.1002/rcm.3633...
). In a literature review encompassing 2007-2009, Boecklen et al. (2011Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics 42: 411-440. https://doi.org/10.1146/annurev-ecolsys-102209-144726
https://doi.org/10.1146/annurev-ecolsys-...
) reviewed the main studies in trophic ecology using stable isotopes. Birds were the fifth most studied group, particularly the ones inhabiting aquatic (ocean, estuaries, lake) and temperate environments (e.g., grassland, forest) (Boecklen et al. 2011Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics 42: 411-440. https://doi.org/10.1146/annurev-ecolsys-102209-144726
https://doi.org/10.1146/annurev-ecolsys-...
). The representation of tropical birds in the literature was less than 10%, highlighting the urgency to apply stable isotopes in new studies to investigate bird ecology, particularly in terrestrial tropical environments.

Several studies have already been undertaken to compile the different facets of stable isotopes as a tool to understand bird ecology (e.g., Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
, Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
, Wiley et al. 2017Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109.). None has focused on the Brazilian fauna, which is very distinct from the North American and European faunas. In this contribution, we discuss the potential of stable isotope studies in Brazil to better understand the ecology of terrestrial birds (Fig. 1).

Figure 1
Flowchart of potential study themes (in bold) to be developed in isotopic ecology with terrestrial birds in Brazil. Each theme branches into several sub-themes that can be explored (first boxes below the themes) and the methods and approaches that can be employed to develop the studies (within the dashed boxes). Many methods and approaches are interchangeable among themes and subthemes (represented by the horizontal arrow). In addition, the shortcomings of stable isotope ecology that should be considered before or during the development of the studies.

What are stable isotopes and how to measure it (C, N, H, O)

Stable isotopes are the non-radioactive forms of the same element that contain different numbers of neutrons. The neutron-depleted isotope is usually called “light” and the neutron-enriched isotope is named “heavy”. Although the amount of each stable isotope in each ecosystem varies naturally, the light isotopes are generally more common than the heavy isotopes (Fry 2008Fry B (2008) Stable Isotope Ecology. Springer, New York, 316 pp.). The sentence “You are what you eat (plus a few per thousand)” represents the use of stable isotope analysis in ecology (DeNiro and Epstein 1976DeNiro MJ, Epstein S (1976) You are what you eat (plus a few ‰): the carbon isotope cycle in food chains. Geological Society of America 6: 834.), meaning that organisms express the isotopic value of the resources they consume (but see Dodds et al. (2014Dodds WK, Collins SM, Hamilton SK, Tank JL, Johnson S, Webster JR, Simon KS, Whiles MR, Rantala HM, McDowell WH, Peterson SD, Riis T, Crenshaw CL, Thomas SA, Kristensen PB, Cheever BM, Flecker AS, Griffiths NA, Crowl T, Rosi-Marshall EJ, El-Sabaawi R, Martí E (2014) You are not always what we think you eat: selective assimilation across multiple whole-stream isotopic tracer studies. Ecology 95(10): 2757-2767. https://doi.org/10.1890/13-2276.1
https://doi.org/10.1890/13-2276.1...
) and Petta et al. (2020Petta JC, Shipley ON, Wintner SP, Cliff G, Dicken ML, Hussey NE (2020) Are you really what you eat? Stomach content analysis and stable isotope ratios do not uniformly estimate dietary niche characteristics in three marine predators. Oecologia 192(4): 1111-1126. https://doi.org/10.1007/s00442-020-04628-6
https://doi.org/10.1007/s00442-020-04628...
) for another viewpoint). Considering that the abundance of isotopes varies from one place to another, the proportion of each isotope in living organisms will also vary geographically. By analyzing different animal tissues with a mass spectrometer, it is possible to measure the proportion of each isotope in them, allowing the calculation of a ratio between heavy/light isotopes. The delta notation (δ) is used to describe the isotopic ratio of a sample as parts per thousand (per mille, ‰), following the equation ‘δX= (Rsample/Rstandard − 1)’, where X is the measured isotope of the element, R is the absolute isotopic ratio (R = heavy/light isotope) and Rstandard is the isotopic ratio of the international standard for each element (e.g., V-PDB for carbon; atmospheric air for nitrogen; V-SMOW for hydrogen and oxygen). The use of Rstandard is to standardize the values of δX to compare among the most different samples since δX will always be enriched or depleted regarding the heavier element (Bond and Hobson 2012Bond AL, Hobson KA (2012) Reporting stable-isotope ratios in ecology: recommended terminology, guidelines and best practices. Waterbirds 35(2): 324. https://doi.org/10.1675/063.035.0213
https://doi.org/10.1675/063.035.0213...
).

Stable carbon isotopes (12C and 13C ratio; denominated as δ13C) are commonly used to determine the habitat and resource use by an organism (Kelly 2000Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78(1): 1-27., Symes 2012Symes CT (2012) Stable Isotope Research in Southern African Birds. In: Ali M (Ed.) Diversity of Ecosystems. IntechOpen, London, 251-288., Wiley et al. 2017Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109., Magioli et al. 2019Magioli M, Moreira MZ, Fonseca RCB, Ribeiro MC, Rodrigues MG, Ferraz KMPMB (2019) Human-modified landscapes alter mammal resource and habitat use and trophic structure. Proceedings of the National Academy of Sciences 116(37): 18466-18472. https://doi.org/10.1073/pnas.1904384116
https://doi.org/10.1073/pnas.1904384116...
). Terrestrial environments are highly associated with land use and cover (e.g., forest formation, anthropogenic areas), and plants vary in their isotopic values according to the photosynthetic cycle (C3, C4 e CAM). Tropical forests are mainly dominated by C3 plants (usually trees), while C4 plants are grasses associated with savannas and agricultural areas (e.g., pasture, sugarcane, maize). Neotropical C3 plants have a wide range of isotopic values from -24‰ to -38‰, while C4 plants range from -11‰ to -15‰ (Martinelli et al. 2009Martinelli LA, Ometto JPHB, Ferraz ES, Victoria RL, Camargo PB, Moreira MZ (2009) Desvendando questões ambientais com isótopos estáveis. Oficina de textos, São Paulo, 144 pp., 2020Martinelli LA, Nardoto GB, Soltangheisi A, Reis CRG, Abdalla-Filho AL, Camargo PB, Domingues TF, Faria D, Figueira AM, Gomes TF, Lins SRM, Mardegan SF, Mariano E, Miatto RC, Moraes R, Moreira MZ, Oliveira RS, Ometto JPHB, Santos FLS, Sena-Souza J, Silva DML, Silva JCSS, Vieira SA (2020) Determining ecosystem functioning in Brazilian biomes through foliar carbon and nitrogen concentrations and stable isotope ratios. Biogeochemistry 117(43): 26842-26848. https://doi.org/10.1007/s10533-020-00714-2
https://doi.org/10.1007/s10533-020-00714...
). Thus, through the values of δ13C, it is possible to determine the environments used by birds, their food sources, and to compare the importance of forests versus anthropogenic areas in the ecology of a species (Ferger et al. 2013Ferger SW, Bohning-Gaese K, Wilcke W, Oelmann Y, Schleuning M (2013) Distinct carbon sources indicate strong differentiation between tropical forest and farmland bird communities. Oecologia 171: 473-486. https://doi.org/10.1007/s00442-012-2422-9
https://doi.org/10.1007/s00442-012-2422-...
, Boesing et al. 2021Boesing AL, Marques TS, Martinelli LA, Nichols E, Siqueira PR, Beier C, Camargo PB, Metzger JP (2021) Conservation implications of a limited avian cross-habitat spillover in pasture lands. Biological Conservation 253: 108898. https://doi.org/10.1016/j.biocon.2020.108898
https://doi.org/10.1016/j.biocon.2020.10...
, Navarro et al. 2021bNavarro AB, Magioli M, Bogoni JA, Moreira MZ, Silveira LF, Alexandrino ER, Luz DTA, Pizo MA, Silva WR, Oliveira VC, Donatelli RJ, Christianini AV, Piratelli AJ, Ferraz KMPMB (2021b) Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196: 171-184. https://doi.org/10.1007/s00442-021-04908-9
https://doi.org/10.1007/s00442-021-04908...
). Nevertheless, in addition to the isotopic variation according to the photosynthetic cycle, other factors (i.e., water stress, light intensity, soil) can also influence the δ13C values of plants (Chesson et al. 2018Chesson LA, Barnette JE, Bowen GJ, Brooks JR, Casale JF, Cerling TE, Cook CS, Douthitt CB, Howa JD, Hurley JM, Kreuzer HW, Lott MJ, Martinelli LA, O’Grady SP, Podlesak DW, Tipple BJ, Valenzuela LO, West JB (2018) Applying the principles of isotope analysis in plant and animal ecology to forensic science in the Americas. Oecologia 187: 1077-1094. https://doi.org/10.1007/s00442-018-4188-1
https://doi.org/10.1007/s00442-018-4188-...
, Sena-Souza et al. 2019Sena-Souza JP, Costa FJV, Nardoto GB (2019) Background and the use of isoscapes in the Brazilian context: essential tool for isotope data interpretation and natural resource management. Ambiente e Agua - An Interdisciplinary Journal of Applied Science 14(2): 1. https://doi.org/10.4136/ambi-agua.2282
https://doi.org/10.4136/ambi-agua.2282...
). Therefore, it is crucial to consider the environmental conditions of the study site when collecting bird samples for isotopic analysis.

Nitrogen isotopes (14N and 15N ratio; denominated as δ15N) are usually employed in studies of the dietary patterns and trophic processes. The ratio of nitrogen stable isotopes tends to be enriched by 3-4‰ as it moves towards the higher levels of the trophic chain. Consequently, top predators are expected to have higher δ15N values than primary consumers (Post 2002Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83(3): 703. https://doi.org/10.2307/3071875
https://doi.org/10.2307/3071875...
), making nitrogen isotope analysis an adequate tool to understand bird diet, the dietary differences among species or foraging groups, and trophic structuring (Herrera et al. 2003Herrera LG, Hobson KA, Rodríguez M, Hernandez P (2003) Trophic partitioning in tropical rain forest birds: insights from stable isotope analysis. Oecologia 136(3): 439-444. https://doi.org/10.1007/s00442-003-1293-5
https://doi.org/10.1007/s00442-003-1293-...
, McKinnon et al. 2017McKinnon EA, Kurt Kyser T, Stutchbury BJM (2017) Does the proportion of arthropods versus fruit in the diet influence overwintering condition of an omnivorous songbird? Journal of Field Ornithology 88(1): 65-79. https://doi.org/10.1111/jofo.12187
https://doi.org/10.1111/jofo.12187...
, English et al. 2018English PA, Green DJ, Nocera JJ (2018) Stable isotopes from museum specimens may provide evidence of long-term change in the trophic ecology of a migratory aerial insectivore. Frontiers in Ecology and Evolution 6: 14. https://doi.org/10.3389/fevo.2018.00014
https://doi.org/10.3389/fevo.2018.00014...
, Navarro et al. 2021bNavarro AB, Magioli M, Bogoni JA, Moreira MZ, Silveira LF, Alexandrino ER, Luz DTA, Pizo MA, Silva WR, Oliveira VC, Donatelli RJ, Christianini AV, Piratelli AJ, Ferraz KMPMB (2021b) Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196: 171-184. https://doi.org/10.1007/s00442-021-04908-9
https://doi.org/10.1007/s00442-021-04908...
). Recently, new data has been published concerning the influence of nitrogen fertilizers on the δ15N values of birds inhabiting anthropogenic areas (Hebert and Wassenaar 2001Hebert CE, Wassenaar LI (2001) Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. Environmental Science and Technology 35(17): 3482-3487. https://doi.org/10.1021/es001970p
https://doi.org/10.1021/es001970p...
, Møller et al. 2018Møller AP, Laursen K, Hobson KA (2018) Retrospectively analysing condition in historical samples of birds. Journal of Zoology 305(3): 188-195. https://doi.org/10.1111/jzo.12551
https://doi.org/10.1111/jzo.12551...
). Synthetic and organic nitrogen fertilizers have distinct δ15N values due to the different nitrogen sources used for their production. The synthetic fertilizers have isotopic values closer to zero, since they are produced with nitrogen from atmospheric air, while those made from organic matter (e.g., animal waste) expresses greater δ15N (Hebert and Wassenaar 2001Hebert CE, Wassenaar LI (2001) Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. Environmental Science and Technology 35(17): 3482-3487. https://doi.org/10.1021/es001970p
https://doi.org/10.1021/es001970p...
). In view of this data, nitrogen isotopes may be useful to clarify the effects of increased anthropogenic pollution, agriculture expansion and urbanization, on the diet of birds (Caron-Beaudoin et al. 2013Caron-Beaudoin É, Gentes ML, Patenaude-Monette M, Hélie JF, Giroux JF, Verreault J (2013) Combined usage of stable isotopes and GPS-based telemetry to understand the feeding ecology of an omnivorous bird, the Ring-billed Gull (Larus delawarensis). Canadian Journal of Zoology 91(10): 689-697.).

The stable isotopes of hydrogen (1H and 2H ratio; denominated as δ2H) and oxygen (16O and 18O ratio; denominated as δ18O) can be used to uncover the geographic and migratory patterns of birds (Hobson 1999Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314-326., 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
, Fox and Bearhop 2008Fox T, Bearhop S (2008) The use of stable-isotope ratios in ornithology. British Birds 101(3): 112-130., Hobson et al. 2019Hobson KA, Wassenaar LI, Bowen GJ, Courtiol A, Trueman CN, Voigt CC, West JB, McMahon KW, Newsome SD (2019) Outlook for Using Stable Isotopes in Animal Migration Studies. In: Hobson KA, Wassenaar LI (Eds) Tracking animal migration with stable isotopes . Academic Press, London , 237-244.). The values of δ2H and δ18O vary according to latitude, precipitation patterns, temperature, elevation, and relative humidity, following the characteristics of the hydrologi cal cycle in each geographic portion of the Earth (Rubenstein and Hobson 2004Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19(5): 256-63. https://doi.org/10.1016/j.tree.2004.03.017
https://doi.org/10.1016/j.tree.2004.03.0...
). The main sources of H and O isotopes in animal tissues are drinking water and water from the food they consume, but O isotopes also derive from the O2 respiration process (Chesson et al. 2018Chesson LA, Barnette JE, Bowen GJ, Brooks JR, Casale JF, Cerling TE, Cook CS, Douthitt CB, Howa JD, Hurley JM, Kreuzer HW, Lott MJ, Martinelli LA, O’Grady SP, Podlesak DW, Tipple BJ, Valenzuela LO, West JB (2018) Applying the principles of isotope analysis in plant and animal ecology to forensic science in the Americas. Oecologia 187: 1077-1094. https://doi.org/10.1007/s00442-018-4188-1
https://doi.org/10.1007/s00442-018-4188-...
). The values of δ2H and δ18O are usually represented as isoscapes, which are the isotopic values of landscapes. However, the analysis of δ13C and δ15N values has increased in studies involving birds and isoscapes (Hobson et al. 2012Hobson KA, Van Wilgenburg SL, Wassenaar LI, Powell RL, Still CJ, Craine JM (2012) A multi-isotope (δ13C, δ15N, δ2H) feather isoscape to assign Afrotropical migrant birds to origins. Ecosphere 3(5): 1-20. https://doi.org/10.1890/ES12-00018.1
https://doi.org/10.1890/ES12-00018.1...
, Cheesman and Cernusak 2016Cheesman AW, Cernusak LA (2016) Isoscapes: A new dimension in community ecology. Tree Physiology 36(12): 1456-1459. https://doi.org/10.1093/treephys/tpw099
https://doi.org/10.1093/treephys/tpw099...
, John Glew et al. 2018John Glew KS, Wanless S, Harris MP, Daunt F, Erikstad KE, Strøm H, Trueman CN (2018) Moult location and diet of auks in the north sea inferred from coupled light-based and isotope-based geolocation. Marine Ecology Progress Series 599: 239-251. https://doi.org/10.3354/meps12624
https://doi.org/10.3354/meps12624...
). Investigations on the association among different isoscapes are promising to promote a better understanding of the migratory patterns of terrestrial birds.

Factors affecting isotopic values in individuals and their environment

The use of stable isotopes in terrestrial ornithological studies is increasing, and results are promising. Certain methodologi cal precautions, however, need to be taken before the analysis of samples and discussion of results (Rubenstein and Hobson 2004Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19(5): 256-63. https://doi.org/10.1016/j.tree.2004.03.017
https://doi.org/10.1016/j.tree.2004.03.0...
, Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
, Ben-David and Flaherty 2012Ben-David M, Flaherty EA (2012) Stable isotopes in mammalian research: a beginner’s guide. Journal of Mammalogy 93(2): 312-328. https://doi.org/10.1644/11-mamm-s-166.1
https://doi.org/10.1644/11-mamm-s-166.1...
). First, a minimal understanding of the natural history and ecology of the species (e.g., animal or plant-based diet, trophic guild, habitat preference) is fundamental to correctly interpret isotopic values. Animals showing similar isotopic values do not necessarily have the same diet, habitat use, or origin (Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
). For example, it is possible to misinterpret data collected from nectarivore birds when the researcher does not consider a priori information on the influence of diet and physiology on δ15N: although hummingbirds may express high δ15N values because they supplement their diet with arthropods (mainly spiders and flies) to meet their high metabolic requirements (Hardesty 2009Hardesty J (2009) Using nitrogen-15 to examine protein sources in hummingbird diets. Ornitología Colombiana 8: 19-28.), resulting in isotopic values that are similar to those found in strict insectivores, their primary food resource is in fact nectar.

Concerning the incorporation of food nutrients into animal tissues, it is important to remember that several biochemical reactions occur in organisms and in the ecosystems, leading to a process known as isotopic discrimination or more specifically, trophic discrimination factor (TDF). This biological process generates differences in isotopic values between the consumer and the resource consumed, which explains the “... (plus a few per mil)” in the sentence previously described (DeNiro and Epstein 1976DeNiro MJ, Epstein S (1976) You are what you eat (plus a few ‰): the carbon isotope cycle in food chains. Geological Society of America 6: 834.). Each food source along with its stable isotopes are incorporated into the tissues of different organisms through different metabolic pathways. Consequently, the TDFs vary according to the tissue and the diet consumed (Healy et al. 2018Healy K, Guillerme T, Kelly SBAA, Inger R, Bearhop S, Jackson AL (2018) SIDER: An R package for predicting trophic discrimination factors of consumers based on their ecology and phylogenetic relatedness. Ecography 41(8): 1393-1400. https://doi.org/10.1111/ecog.03371
https://doi.org/10.1111/ecog.03371...
). Additionally, the dynamics of isotopic incorporation vary among animal tissues, depending on physiological processes. Since the synthesis and replacement of each tissue of an animal will happen within a different period in time, it is possible to use multi-tissue analysis to uncover the consumption of resources at distinct phases of the life of an organism (Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
). In the case of birds, while some tissues reflect the isotopic value of the resources consumed a few days ago (e.g., blood plasma, liver), others reflect the resources consumed months or years before (e.g., feathers, claws, bone collagen) (Hobson and Clark 1992Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I : Turnover of 13C in tissues. Condor 94(1): 181-188., Bearhop et al. 2003Bearhop S, Furness RW, Hilton GM, Votier SC, Waldron S (2003) A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Functional Ecology 17(2): 270-275. https://doi.org/10.1046/j.1365-2435.2003.00725.x
https://doi.org/10.1046/j.1365-2435.2003...
). The discrimination and dynamics of isotopic incorporation may vary according to the species’ phylogenetic relationships or similarity in dietary patterns (e.g., herbivores, carnivores, omnivores), highlighting the importance of carefully considering the use of correction factors (e.g., TDF) in bird isotopic ecology.

Another important consideration is to collect and create a comprehensive baseline of food resources (Post 2002Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83(3): 703. https://doi.org/10.2307/3071875
https://doi.org/10.2307/3071875...
). The baseline can be measured through the direct isotopic analysis of items consumed by the species or using phylogenetically related organisms as a proxy for resources (Casey and Post 2011Casey MM, Post DM (2011) The problem of isotopic baseline: Reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106(1-2): 131-148. https://doi.org/10.1016/j.earscirev.2011.02.001
https://doi.org/10.1016/j.earscirev.2011...
). Creating a good baseline ensures that the isotopic comparisons among individuals are accurate, especially in dietary and food-web studies. In long-term studies, it may be difficult to sample historical resources to compose a baseline of the past. In this case, researchers should resort to museum collections in search of food items, or develop a robust proxy for the historical baseline (e.g., English et al. 2018English PA, Green DJ, Nocera JJ (2018) Stable isotopes from museum specimens may provide evidence of long-term change in the trophic ecology of a migratory aerial insectivore. Frontiers in Ecology and Evolution 6: 14. https://doi.org/10.3389/fevo.2018.00014
https://doi.org/10.3389/fevo.2018.00014...
, Mason et al. 2020Mason NA, Unitt P, Sparks JP (2020) Agriculture induces isotopic shifts and niche contraction in Horned Larks (Eremophila alpestris) of the Colorado Desert. Journal of Ornithology 162: 381-393. https://doi.org/10.1007/s10336-020-01834-0
https://doi.org/10.1007/s10336-020-01834...
). In Brazil, where biodiversity is high, a single bird species can consume many different food items (Durães and Marini 2005Durães R, Marini MAÂ (2005) A quantitative assessment of bird diets in the Brazilian Atlantic Forest, with recommendations for future diet studies. Ornitología Neotropical 16: 65-83., Lopes et al. 2005Lopes LE, Fernandes AM, Marini MÂ (2005) Diet of some Atlantic Forest birds. Ararajuba 13(1): 95-103., Siqueira et al. 2015Siqueira PR, Vasconcelos MF, Gonçalves RMM, Leite LO (2015) Assessment of stomach contents of some amazonian birds. Ornitología Neotropical 26: 79-88.). Thus, collecting and analyzing the complete baseline of a species may be unfeasible, highlighting the importance of developing good proxies from phylogenetically related organisms.

The diversity of environmental characteristics among biomes in Brazil (e.g., precipitation, vegetation type, soil, landscape composition) is also a reason for caution when investigating patterns in the isotopic ecology of birds. To be able to understand how abiotic factors influence species’ isotopic values, it is important to examine refined isoscape maps for the Brazilian territory, which already incorporate several environmental variables in their models (Sena-Souza et al. 2019Sena-Souza JP, Costa FJV, Nardoto GB (2019) Background and the use of isoscapes in the Brazilian context: essential tool for isotope data interpretation and natural resource management. Ambiente e Agua - An Interdisciplinary Journal of Applied Science 14(2): 1. https://doi.org/10.4136/ambi-agua.2282
https://doi.org/10.4136/ambi-agua.2282...
). Vegetation from distinct regions can also express isotopic variation or similarity (Vitória et al. 2018Vitória AP, Ávila-Lovera E, Oliveira Vieira T, Couto-Santos APL, Pereira TJ, Funch LS, Freitas L, Miranda LDAP, Rodrigues PJFP, Rezende CE, Santiago LS (2018) Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) of deciduous and evergreen understorey trees in two tropical Brazilian Atlantic forests. Journal of Tropical Ecology 34(2): 145-156. https://doi.org/10.1017/S0266467418000093
https://doi.org/10.1017/S026646741800009...
, Martinelli et al. 2020Martinelli LA, Nardoto GB, Soltangheisi A, Reis CRG, Abdalla-Filho AL, Camargo PB, Domingues TF, Faria D, Figueira AM, Gomes TF, Lins SRM, Mardegan SF, Mariano E, Miatto RC, Moraes R, Moreira MZ, Oliveira RS, Ometto JPHB, Santos FLS, Sena-Souza J, Silva DML, Silva JCSS, Vieira SA (2020) Determining ecosystem functioning in Brazilian biomes through foliar carbon and nitrogen concentrations and stable isotope ratios. Biogeochemistry 117(43): 26842-26848. https://doi.org/10.1007/s10533-020-00714-2
https://doi.org/10.1007/s10533-020-00714...
). For this reason, the isotopic values of the vegetation need to be considered, to correctly interpret the results of studies that incorporate a broad spatial area, especially because many birds have plant-based diets.

Stable isotopes in dietary, niche and food web studies

Stable isotopes can be broadly used in trophic ecology and foraging studies, for instance: estimating the proportion of items in the diet, assessing which environment is used more often to obtain food and as habitat, measuring different isotopic niche dimensions, and investigating foraging specializations among individuals, species, or groups (Table 1). Most dietary studies employ the stable carbon (δ13C) and nitrogen (δ15N) isotopes, which give more information on habitat and resource use, and the trophic levels of animal species (Kelly 2000Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78(1): 1-27., Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
).

Table 1
Examples of studies using stable isotope analysis to cover relevant themes and sub-themes of terrestrial bird ecology. The preference adopted for citation in the table was the existence of studies developed in Brazil or the Neotropics. We also cite studies from temperate regions that have not yet been developed in the Neotropics, showing the potential of development in Brazil.

The ingestion of many food resources by an organism can be measured with stable isotope mixing models, which estimate how much each food source contributes to the diet of the individual’s (Phillips and Gregg 2003Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261-269. https://doi.org/10.1007/s00442-003-1218-3
https://doi.org/10.1007/s00442-003-1218-...
, Phillips 2012Phillips DL (2012) Converting isotope values to diet composition: the use of mixing models. Journal of Mammalogy 93(2): 342-352. https://doi.org/10.1644/11-MAMM-S-158.1
https://doi.org/10.1644/11-MAMM-S-158.1...
). There are several mixing models that can be used to ascertain foraging patterns. Currently, the Bayesian models are favored, since they fully incorporate sources of uncertainty (but see Hopkins and Ferguson (2012Hopkins JB, Ferguson JM (2012) Estimating the diets of animals using stable isotopes and a comprehensive Bayesian mixing model. PLoS One 7(1): e28478. https://doi.org/10.1371/journal.pone.0028478
https://doi.org/10.1371/journal.pone.002...
) and Stock et al. (2018Stock BC, Jackson AL, Ward EJ, Parnell AC, Phillips DL, Semmens BX (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6: e5096. https://doi.org/10.7717/peerj.5096
https://doi.org/10.7717/peerj.5096...
) for some different models and their particularities). González-Carcacía et al. (2020González-Carcacía JA, Gerardo Herrera LM, Nassar JM (2020) Dietary importance of C3 and CAM food pathways for birds in a Neotropical semiarid zone. Biotropica 52(5): 938-945. https://doi.org/10.1111/btp.12798
https://doi.org/10.1111/btp.12798...
) used mixing models to unravel the greater contribution of C3 plants (mainly forest-based) over CAM plants (cactus and agaves) in the diet of Neotropical birds in a semi-arid zone in Venezuela. Their results revealed the importance of forest patches for bird communities. Guaraldo et al. (2019Guaraldo AC, Kelly JF, Marini MÂ (2019) Independent trophic behavior and breeding success of a resident flycatcher and a coexisting migratory congener. Austral Ecology 44(1): 126-137. https://doi.org/10.1111/aec.12660
https://doi.org/10.1111/aec.12660...
) evaluated the diet of two congener species of Elaenia Sundevall, 1836 (one resident and one migratory) over their annual life cycles in the Brazilian Cerrado. Using mixing models, the authors showed that both species employ similar foraging strategies, contrary to the expectation that their diets would differ. Their study brings attention to the importance of new research to assess differences and similarities in the diet of birds that co-occur in species-rich tropical biomes. Mixing models encompass a wide range of research possibilities, but it is crucial to have a good experimental design for sample collection (both from birds and their food resources), and a prior knowledge of the analysis to be employed and its particularities (Phillips et al. 2014Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92(10): 823-835. https://doi.org/10.1139/cjz-2014-0127
https://doi.org/10.1139/cjz-2014-0127...
, Newton 2016Newton J (2016) Stable Isotopes as Tools inEcological Research. In: eLS Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, 1-8. https://doi.org/10.1002/9780470015902.a0021231.pub2
https://doi.org/10.1002/9780470015902.a0...
). Especially in Brazil, where there is a great diversity of species and food resources, it is important to sample all possible food items to build an adequate isotopic baseline.

In addition to specifying the contribution of each food item to the diet of a species, stable isotopes in trophic ecology studies are also employed to assess which habitat is used by an animal to obtain resources (e.g., Guaraldo et al. 2016Guaraldo AC, Kelly JF, Marini MÂ (2016) Contrasting annual cycles of an intratropical migrant and a tropical resident bird. Journal of Ornithology 157(3): 695-705. https://doi.org/10.1007/s10336-016-1327-5
https://doi.org/10.1007/s10336-016-1327-...
, Magioli et al. 2019Magioli M, Moreira MZ, Fonseca RCB, Ribeiro MC, Rodrigues MG, Ferraz KMPMB (2019) Human-modified landscapes alter mammal resource and habitat use and trophic structure. Proceedings of the National Academy of Sciences 116(37): 18466-18472. https://doi.org/10.1073/pnas.1904384116
https://doi.org/10.1073/pnas.1904384116...
, González-Carcacía et al. 2020González-Carcacía JA, Gerardo Herrera LM, Nassar JM (2020) Dietary importance of C3 and CAM food pathways for birds in a Neotropical semiarid zone. Biotropica 52(5): 938-945. https://doi.org/10.1111/btp.12798
https://doi.org/10.1111/btp.12798...
). The habitat-level approach in foraging studies is important because it can serve as a guide for conservation, especially in landscapes that have been extremely modified by man. For instance, the isotopic results of Boesing et al. (2021Boesing AL, Marques TS, Martinelli LA, Nichols E, Siqueira PR, Beier C, Camargo PB, Metzger JP (2021) Conservation implications of a limited avian cross-habitat spillover in pasture lands. Biological Conservation 253: 108898. https://doi.org/10.1016/j.biocon.2020.108898
https://doi.org/10.1016/j.biocon.2020.10...
) highlight the urgency to preserve forest patches and to design multifunctional landscapes for the maintenance of bird communities. Another consideration is that generalist species of the Brazilian Atlantic Forest, which appear to adapt well to environmental changes, in fact consume forest resources (mainly C3 plants) more than they consume resources from agricultural areas (C4 plants) (Boesing et al. 2021Boesing AL, Marques TS, Martinelli LA, Nichols E, Siqueira PR, Beier C, Camargo PB, Metzger JP (2021) Conservation implications of a limited avian cross-habitat spillover in pasture lands. Biological Conservation 253: 108898. https://doi.org/10.1016/j.biocon.2020.108898
https://doi.org/10.1016/j.biocon.2020.10...
, Navarro et al. 2021bNavarro AB, Magioli M, Bogoni JA, Moreira MZ, Silveira LF, Alexandrino ER, Luz DTA, Pizo MA, Silva WR, Oliveira VC, Donatelli RJ, Christianini AV, Piratelli AJ, Ferraz KMPMB (2021b) Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196: 171-184. https://doi.org/10.1007/s00442-021-04908-9
https://doi.org/10.1007/s00442-021-04908...
). Nevertheless, the dependence of birds on forest habitats is not exclusive to the Neotropics. Ferger et al. (2013Ferger SW, Bohning-Gaese K, Wilcke W, Oelmann Y, Schleuning M (2013) Distinct carbon sources indicate strong differentiation between tropical forest and farmland bird communities. Oecologia 171: 473-486. https://doi.org/10.1007/s00442-012-2422-9
https://doi.org/10.1007/s00442-012-2422-...
), in a study using carbon isotopic values, discussed the importance of forests as a source of food for bird communities in Central Africa. Even though granivores are adapted to open environments (showing δ13C values similar to C4 plants), many other trophic guilds are highly dependent on forest resources, especially understory insectivores (Ferger et al. 2013Ferger SW, Bohning-Gaese K, Wilcke W, Oelmann Y, Schleuning M (2013) Distinct carbon sources indicate strong differentiation between tropical forest and farmland bird communities. Oecologia 171: 473-486. https://doi.org/10.1007/s00442-012-2422-9
https://doi.org/10.1007/s00442-012-2422-...
). In a world facing rapid human-induced changes in landscape composition and structure, stable isotope analysis may help to better understand the various ecological aspects of birds in highly modified habitats.

Studies in trophic ecology may estimate the isotopic niche metrics of bird species. Understanding a species’ niche, which includes diet, habitat use, and geographic patterns, is very important to understand the natural history of a species (McGill et al. 2006McGill B, Enquist B, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21(4): 178-185. https://doi.org/10.1016/j.tree.2006.02.002
https://doi.org/10.1016/j.tree.2006.02.0...
). The isotopic niche is correlated with the ecological niche, since the δ-space is comparable to the n-dimensional space of the niche concept (Newsome et al. 2007Newsome SD, Martínez del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5(8): 429-436. https://doi.org/10.1890/060150.01
https://doi.org/10.1890/060150.01...
). Bosenbecker and Bugoni (2020Bosenbecker C, Bugoni L (2020) Trophic niche similarities of sympatric Turdus thrushes determined by fecal contents, stable isotopes, and bipartite network approaches. Ecology and Evolution 10(17): 9073-9084. https://doi.org/10.1002/ece3.6485
https://doi.org/10.1002/ece3.6485...
) investigated isotopic niche width and overlap in three sympatric species of Turdus Linnaeus, 1758 in southern Brazil. Even though the contribution of each food item is slightly different among thrushes, niche overlap shows that the three species share similar resources, mainly C3 plants and invertebrates (Bosenbecker and Bugoni 2020Bosenbecker C, Bugoni L (2020) Trophic niche similarities of sympatric Turdus thrushes determined by fecal contents, stable isotopes, and bipartite network approaches. Ecology and Evolution 10(17): 9073-9084. https://doi.org/10.1002/ece3.6485
https://doi.org/10.1002/ece3.6485...
). Navarro et al. (2021bNavarro AB, Magioli M, Bogoni JA, Moreira MZ, Silveira LF, Alexandrino ER, Luz DTA, Pizo MA, Silva WR, Oliveira VC, Donatelli RJ, Christianini AV, Piratelli AJ, Ferraz KMPMB (2021b) Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196: 171-184. https://doi.org/10.1007/s00442-021-04908-9
https://doi.org/10.1007/s00442-021-04908...
) documented a decrease in the width of the isotopic niche of many trophic guilds in human-modified landscapes when compared to birds in natural areas of the Atlantic Forest biome. Although the niche of granivore birds tends to expand in human-modified landscapes, the niche of frugivore, insectivore, nectarivore, and omnivore birds becomes narrower in response to the anthropogenic impacts in southeastern Brazil (Navarro et al. 2021bNavarro AB, Magioli M, Bogoni JA, Moreira MZ, Silveira LF, Alexandrino ER, Luz DTA, Pizo MA, Silva WR, Oliveira VC, Donatelli RJ, Christianini AV, Piratelli AJ, Ferraz KMPMB (2021b) Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196: 171-184. https://doi.org/10.1007/s00442-021-04908-9
https://doi.org/10.1007/s00442-021-04908...
). Several Brazilian biomes have struggled with human expansion and, consequently, with their negative environmental effects, such as habitat loss, fragmentation, and savannization (e.g., Ribeiro et al. 2009Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142(6): 1141-1153. https://doi.org/10.1016/j.biocon.2009.02.021
https://doi.org/10.1016/j.biocon.2009.02...
, Carvalho et al. 2009Carvalho FMV, De Marco P, Ferreira LG (2009) The Cerrado into-pieces: Habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biological Conservation 142(7): 1392-1403. https://doi.org/10.1016/j.biocon.2009.01.031
https://doi.org/10.1016/j.biocon.2009.01...
, Silvério et al. 2013Silvério DV, Brando PM, Balch JK, Putz FE, Nepstad DC, Oliveira-Santos C, Bustamante MMC (2013) Testing the Amazon savannization hypothesis: fire effects on invasion of a neotropical forest by native cerrado and exotic pasture grasses. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20120427. https://doi.org/10.1098/rstb.2012.0427
https://doi.org/10.1098/rstb.2012.0427...
, Sales et al. 2020Sales LP, Galetti M, Pires MM (2020) Climate and land-use change will lead to a faunal “savannization” on tropical rainforests. Global Change Biology 26(12): 7036-7044. https://doi.org/10.1111/gcb.15374
https://doi.org/10.1111/gcb.15374...
, Magioli et al. 2021Magioli M, Ferraz KMPMB, Chiarello AG, Galetti M, Setz EZF, Paglia AP, Abrego N, Ribeiro MC, Ovaskainen O (2021) Land-use changes lead to functional loss of terrestrial mammals in a Neotropical rainforest. Perspectives in Ecology and Conservation 19(2): 161-170. https://doi.org/10.1016/j.pecon.2021.02.006
https://doi.org/10.1016/j.pecon.2021.02....
). Contrasting with this situation, little has been done in the field of isotopic niche studies to produce information that could guide the conservation of bird species and their habitats in the Neotropical region.

The isotopic niche approach provides practical solutions to several questions regarding the ecology of birds. Nevertheless, it is worth mentioning that this method, which is backed up by helpful analytical software packages (e.g., SIBER - Jackson et al. 2011Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80(3): 595-602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
https://doi.org/10.1111/j.1365-2656.2011...
, rKIN - Eckrich et al. 2020Eckrich CA, Albeke SE, Flaherty EA, Bowyer RT, Ben-David M (2020) rKIN: Kernel-based method for estimating isotopic niche size and overlap. Journal of Animal Ecology 89(3): 757-771. https://doi.org/10.1111/1365-2656.13159
https://doi.org/10.1111/1365-2656.13159...
), is still recent and has some shortfalls. To avoid them, it is important to make a detailed assessment of the isotopic variation of baseline resources (Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
). Moreover, we do not know the diet of many Neotropical bird species, highlighting the need for a careful interpretation of the results, and expanding our knowledge about the natural history of those species.

Stable isotope analysis has proven a valuable tool to identify foraging specializations in individuals or species (Araújo et al. 2007Araújo MS, Bolnick DI, Machado G, Giaretta AA, Reis SF (2007) Using δ13C Stable Isotopes to Quantify Individual-Level Diet Variation. Oecologia 152(4): 643-654. https://doi.org/10.1007/s00442-007-0687-l
https://doi.org/10.1007/s00442-007-0687-...
, Layman et al. 2012Layman CA, Araújo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: An overview of analytical tools. Biological Reviews 87(3): 545-562. https://doi.org/10.1111/j.1469-185X.2011.00208.x
https://doi.org/10.1111/j.1469-185X.2011...
). Species may exhibit varying degrees of intra-population specialization in food resource exploration and habitat use, which can be identified through multi-tissue isotopic analysis (Araújo et al. 2011Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecology Letters 14(9): 948-958. https://doi.org/10.1111/j.1461-0248.2011.01662.x
https://doi.org/10.1111/j.1461-0248.2011...
, Bond et al. 2016Bond AL, Jardine TD, Hobson KA (2016) Multi-tissue stable-isotope analyses can identify dietary specialization. Methods in Ecology and Evolution 7(12): 1428-1437. https://doi.org/10.1111/2041-210X.12620
https://doi.org/10.1111/2041-210X.12620...
). Martínez del Rio et al. (2009aMartínez del Rio C, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009a) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161: 149-159. https://doi.org/10.1007/s00442-009-1357-2
https://doi.org/10.1007/s00442-009-1357-...
) compared intrapopulation isotopic variation among three species of Cinclodes G.R. Gray, 1840 in South America. Each of the species has a seasonal foraging singularity. Representatives of one species are generalists and consume terrestrial/freshwater and marine resources. Individuals of a second species have both generalist and specialist individuals, and a third species has specialist individuals strictly dependent on marine invertebrates (Martínez del Rio et al. 2009aMartínez del Rio C, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009a) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161: 149-159. https://doi.org/10.1007/s00442-009-1357-2
https://doi.org/10.1007/s00442-009-1357-...
). Guaraldo et al. (2019Guaraldo AC, Kelly JF, Marini MÂ (2019) Independent trophic behavior and breeding success of a resident flycatcher and a coexisting migratory congener. Austral Ecology 44(1): 126-137. https://doi.org/10.1111/aec.12660
https://doi.org/10.1111/aec.12660...
) showed that the diet of Elaenia cristata Pelzeln, 1868, a terrestrial migratory bird in Brazil, varies depending on the time of the year (breeding, molting, and non-breeding), and between adults and juveniles. Some birds may have distinct individual dietary preferences, so it is possible to observe isotopic variations among individuals of different ages and sexes (Fox and Bearhop 2008Fox T, Bearhop S (2008) The use of stable-isotope ratios in ornithology. British Birds 101(3): 112-130.). Nevertheless, although Brazil has a vast territory inhabited by several species with different degrees of specialization, stable isotope analysis has not been employed to its full potential to allows us to understand these patterns.

The concept of isoscapes and the use of stable isotopes to track migratory species

Detecting large-scale movement patterns in migratory species may be time consuming and financially costly, especially when conventional methodologies are employed (e.g., telemetry, mark-recapture, leg banding) (Hobson and Norris 2008Hobson KA, Norris DR (2008) Animal migration: a context for using new techniques and approaches. In: Hobson KA, Wassenaar LI (Eds) Tracking animal migration with stable isotopes. Academic Press, London, 1-19.). It is increasingly evident that isotopic analysis is a great cost-effective tool to obtain information on the geographic patterns of birds through the use of isoscapes and individual values of δ2H and δ18O (Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
, Hobson et al. 2019Hobson KA, Wassenaar LI, Bowen GJ, Courtiol A, Trueman CN, Voigt CC, West JB, McMahon KW, Newsome SD (2019) Outlook for Using Stable Isotopes in Animal Migration Studies. In: Hobson KA, Wassenaar LI (Eds) Tracking animal migration with stable isotopes . Academic Press, London , 237-244., Table 1). There has been a growing appeal among researchers to explore Neotropical regions, in association with North America studies, to construct an isotopic atlas for migratory birds (Hobson et al. 2014Hobson KA, Van Wilgenburg SL, Faaborg J, Toms JD, Rengifo C, Sosa AL, Aubry Y, Brito Aguilar R (2014) Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity. Journal of Field Ornithology 85(3): 237-257. https://doi.org/10.1111/jofo.12065
https://doi.org/10.1111/jofo.12065...
). This effort aims to facilitate the understanding of migratory dynamics, and to develop more effective approaches to the conservation of species. Even though Brazil has a great diversity of migratory birds and is also in the migratory route of several species (Somenzari et al. 2018Somenzari M, Amaral PP, Cueto VR, Guaraldo ADC, Jahn AE, Lima DM, Lima PC, Lugarini C, Machado CG, Martinez J, Nascimento JLX, Pacheco JF, Paludo D, Prestes NP, Serafini PP, Silveira LF, Sousa AEBA, Sousa NA, Souza MA, Telino-Júnior WR, Whitney BM (2018) An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia 58: 3. https://doi.org/10.11606/1807-0205/2018.58.03
https://doi.org/10.11606/1807-0205/2018....
), few studies conducted in the country have used stable isotopes to address this theme.

Brazil stretches over a wide latitudinal and longitudinal extent, which provides markedly distinct isoscapes (Sena-Souza et al. 2019Sena-Souza JP, Costa FJV, Nardoto GB (2019) Background and the use of isoscapes in the Brazilian context: essential tool for isotope data interpretation and natural resource management. Ambiente e Agua - An Interdisciplinary Journal of Applied Science 14(2): 1. https://doi.org/10.4136/ambi-agua.2282
https://doi.org/10.4136/ambi-agua.2282...
). Isoscapes are the geographic patterns of isotopic values of landscapes, represented by maps of δ2H, δ18O, and others. The different Brazilian biomes have particular water regimes and, therefore, each may show different values of δ2H and δ18O (Bowen et al. 2005Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143(3): 337-348. https://doi.org/10.1007/s00442-004-1813-y
https://doi.org/10.1007/s00442-004-1813-...
). Although seasonal variations in atmospheric circulation slightly influence in isoscapes annually, isotopic spatial patterns are stable on a large temporal scale, providing robust data to trace the geographic origin of individuals analyzed (Nardoto et al. 2017Nardoto GB, Ribeiro JF, Sena-Souza JP, Guaraldo AC, Saquetti CH (2017) rastreamento forense: uso dos isótopos estáveis no combate ao crime. In: Costa FJV, Ferreira JM, Monteiro KRG, Mayrink RR (Eds) Ciência contra o tráfico: Avanços no combate ao comércio ilegal de animais silvestres. Imprell Gráfica e Editora, João Pessoa, 51-78.).

Migrant birds have different breeding and wintering sites. Usually, they molt during one of these periods, before the migration event. Thus, the values of δ2H and δ18O of the feathers, an inert tissue, reflect the isotopic value of the region in which the molting was performed (Hobson 1999Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314-326.). Certain tropical regions are obligatory routes for several migratory species. If stochastic events and anthropogenic impacts reach these areas, the conservation of the birds passing through these routes may be impacted. Cardenas-Ortiz et al. (2020Cardenas-Ortiz L, Bayly NJ, Kardynal KJ, Hobson KA (2020) Defining catchment origins of a geographical bottleneck: Implications of population mixing and phenological overlap for the conservation of Neotropical migratory birds. Condor 122(2): duaa004. https://doi.org/10.1093/condor/duaa004
https://doi.org/10.1093/condor/duaa004...
) observed that populations of some migratory birds from distinct North American sites mixed spatial-temporally in an area of Colombia. Populations that do not have distinct migratory routes may compete for resources in the same region at the same time, representing a possible bottleneck for the survival of these species (Cardenas-Ortiz et al. 2020Cardenas-Ortiz L, Bayly NJ, Kardynal KJ, Hobson KA (2020) Defining catchment origins of a geographical bottleneck: Implications of population mixing and phenological overlap for the conservation of Neotropical migratory birds. Condor 122(2): duaa004. https://doi.org/10.1093/condor/duaa004
https://doi.org/10.1093/condor/duaa004...
). South America receives many migratory birds escaping from the winter of the Northern Hemisphere. Forest areas in northern Brazil have been impacted by changes in land-use for agricultural purposes, which may pose a threat not only to resident species but also to migrant birds. Using isotopic analysis to track the origin of individuals may be helpful for the determination of priority areas for conservation of paramount sites on migratory routes.

Altitudinal migration is another geographic pattern performed by several Neotropical birds and which can be measured using the isotopic analysis of hydrogen. Variations in precipitation rates and atmospheric dynamics along altitudinal gradients promote different values of δ2H through the environment and, consequently, in migrant individuals (Hobson et al. 2003Hobson KA, Wassenaar LI, Milá B, Lovette I, Dingle C, Smith TB (2003) Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia 136: 302-308.). By analyzing different tissues, it is possible to track the altitudinal migratory route, since each has a distinct turnover rate. This means that each tissue will provide the δ2H value of the environment in which it was formed (e.g., low or high elevation) (Newsome et al. 2015Newsome SD, Sabat P, Wolf N, Rader JA, DelRio CM (2015) Multi-tissue δ2H analysis reveals altitudinal migration and tissue-specific discrimination patterns in Cinclodes. Ecosphere 6(11): 1-18.). Nevertheless, it is fundamental to consider the seasonal variations in the precipitation patterns of a region to correctly interpret the isotopic values of birds (Villegas et al. 2016Villegas M, Newsome SD, Blake JG (2016) Seasonal patterns in δ2H values of multiple tissues from Andean birds provide insights into elevational migration. Ecological Applications 26(8): 2383-2389.). Studies that evaluate altitudinal migration in the Brazilian territory using stable isotopes are recent and are few and far in-between. Adopting this methodology might facilitate the understanding of the elevational movement patterns of birds, especially considering the influence of climate change in modifying the migratory dynamics of species.

Understanding physiological and stressful events that might affect birds through laboratory experiments

The accuracy of isotopic analysis depends on incorporating corrections to individual values that consider the physiological dynamics of the species (Table 1), such as isotopic discrimination. Correctly measuring the discrimination values between consumers and food resources is essential for applying mixing models and estimating the trophic position of individuals (Martínez del Rio et al. 2009bMartínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009b) Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84: 91-111. https://doi.org/10.1111/j.1469-185X.2008.00064.x
https://doi.org/10.1111/j.1469-185X.2008...
). Nonetheless, estimating the discrimination factors is not trivial. Studies have proposed tools to help researchers estimate trophic discrimination factors (TDFs) to correct isotopic values for species, without the need for experimental work (e.g., Caut et al. 2009Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): The effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46(2): 443-453. https://doi.org/10.1111/j.1365-2664.2009.01620.x
https://doi.org/10.1111/j.1365-2664.2009...
, Healy et al. 2018Healy K, Guillerme T, Kelly SBAA, Inger R, Bearhop S, Jackson AL (2018) SIDER: An R package for predicting trophic discrimination factors of consumers based on their ecology and phylogenetic relatedness. Ecography 41(8): 1393-1400. https://doi.org/10.1111/ecog.03371
https://doi.org/10.1111/ecog.03371...
). Still, exploring this theme in further studies is essential to fine-tune the isotopic analysis methodology (Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
), especially concerning Brazil’s native birds, since their TDFs have not, for the most part, been calculated. Through controlled and monitored changes in the diet of individual birds in the laboratory, it is possible to measure the TDF of a species (Bearhop et al. 2002Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors That Influence Assimilation Rates and Fractionation of Nitrogen and Carbon Stable Isotopes in Avian Blood and Feathers. Physiological and Biochemical Zoology 75(5): 451-458. https://doi.org/10.1086/342800
https://doi.org/10.1086/342800...
). In this type of experiment, researchers must give the animals a diet with different isotopic values at preset intervals (e.g., starting with C3 resources and switching to C4) and, concomitantly, monitor the isotopic values of the tissues until the change in the diet can be identified. In these types of experiments, it is important to determine the growth rate of the target tissue for analysis. Ornithologists interested in this topic may rely on zoos and legal breeding programs to develop laboratory experiments, while keeping in mind that the physiological patterns of captive and wild individuals may differ (Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
).

The isotopic turnover of each tissue may vary greatly in time (from days to years) depending on the physiology of the species (Vander Zanden et al. 2015Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS One 10(1): e0116182. https://doi.org/10.1371/journal.pone.0116182
https://doi.org/10.1371/journal.pone.011...
). Several studies have already focused on determining the turnover rates of various tissues of birds and other taxa (Boecklen et al. 2011Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics 42: 411-440. https://doi.org/10.1146/annurev-ecolsys-102209-144726
https://doi.org/10.1146/annurev-ecolsys-...
). Nevertheless, the dynamics of isotopic incorporation among tissues is also a relatively new topic for Brazilian ornithologists. The same approach (switching diets in the laboratory) can be used to monitor the turnover rate of each tissue that one intends to use in the isotopic analysis (Newton 2016Newton J (2016) Stable Isotopes as Tools inEcological Research. In: eLS Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, 1-8. https://doi.org/10.1002/9780470015902.a0021231.pub2
https://doi.org/10.1002/9780470015902.a0...
). Considering that species from diverse Brazilian biomes may present particular physiologies, it is desirable to understand whether they show distinct turnover rates for the same tissue.

There is still no consensus among researchers about the influence of nutritional stress on the isotopic values expressed by bird tissues. Some studies have shown that δ13C and δ15N values can vary slightly or greatly due to stressful events, depending on the physiology of the species (e.g., Hobson et al. 1993Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95(2): 388-394., Graves et al. 2012Graves GR, Newsome SD, Willard DE, Grosshuesch DA, Wurzel WW, Fogel ML (2012). Nutritional stress and body condition in the Great Gray Owl (Strix nebulosa) during winter irruptive migrations. Canadian Journal of Zoology 90(7): 787-797. https://doi.org/10.1139/z2012-047
https://doi.org/10.1139/z2012-047...
). Extreme events such as starvation and natural disasters may have serious physiological consequences for birds, including defects in the feather, for instance fault bars (Ross et al. 2015Ross JD, Kelly JF, Bridge ES, Engel MH, Reinking DL, Boyle WA (2015) Pallid bands in feathers and associated stable isotope signatures reveal effects of severe weather stressors on fledgling sparrows. PeerJ 3: e814. https://doi.org/10.7717/peerj.814
https://doi.org/10.7717/peerj.814...
, Jovani and Rohwer 2017Jovani R, Rohwer S (2017) Fault bars in bird feathers: mechanisms, and ecological and evolutionary causes and consequences. Biological Reviews 92(2): 1113-1127. https://doi.org/10.1111/brv.12273
https://doi.org/10.1111/brv.12273...
). Ross et al. (2015Ross JD, Kelly JF, Bridge ES, Engel MH, Reinking DL, Boyle WA (2015) Pallid bands in feathers and associated stable isotope signatures reveal effects of severe weather stressors on fledgling sparrows. PeerJ 3: e814. https://doi.org/10.7717/peerj.814
https://doi.org/10.7717/peerj.814...
) analyzed juvenile individuals of Ammodramus savannarum (J.F. Gmelin, 1789) after a severe storm, comparing individuals with and without pallid bands (a type of fault bar). Juveniles containing pallid bands showed lower values of δ15N than individuals with normal feathers, due to the environmental stressors they experienced. Other studies point to the lack of a relationship between the isotopic values found in bird tissues and stressful events, such as food restriction and disease infection (e.g., Kempster et al. 2007Kempster B, Zanette L, Longstaffe FJ, MacDougall-Shackleton SA, Wingfield JC, Clinchy M (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151(3): 365-371. https://doi.org/10.1007/s00442-006-0597-7
https://doi.org/10.1007/s00442-006-0597-...
, Yohannes et al. 2011Yohannes E, Palinauskas V, Valkiūnas G, Lee RW, Bolshakov CV, Bensch S (2011) Does avian malaria infection affect feather stable isotope signatures? Oecologia 167(4): 937-942. https://doi.org/10.1007/s00442-011-2041-x
https://doi.org/10.1007/s00442-011-2041-...
). None of these studies have been developed with birds from Brazilian biomes. Thus, ornithologists must make efforts to understand the relationship among physiology, stressful events, and isotopic values of species occurring in Brazil.

Using isotopic analysis to unravel long-term temporal dyna mics in bird ecology

Understanding the historical patterns in the ecology of a bird is essential for the development of conservation practices. To that end, it is possible to obtain broad temporal information through the analysis of stable isotopes. All sub-themes already covered in this review may be subject to studies aimed to understand the history of a bird’s ecology, such as diet, habitat use, and geographic and physiological patterns (Table 1). To that end, natural history museums play a fundamental role in preserving metabolically inert tissues (e.g., feathers, bones, claws) that serve as a source for isotopic analysis (Wiley et al. 2017Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109.). Generally, museum specimens are useful and is the only way to access historical samples (Winker 2005Winker K (2005) Bird Collections: Development and use of a scientific resource. Auk 122(3): 966-971. https://doi.org/10.1093/auk/122.3.966
https://doi.org/10.1093/auk/122.3.966...
).

Although ornithological collections are a rich source of historical samples for the analysis of stable isotopes, museum specimens have not been broadly used in studies, particularly in the Neotropics. Considering the lack of extensive specific literature with isotopes and terrestrial birds on a temporal scale in Brazil, studies from temperate environments will be discussed to illuminate some prospects to be employed in tropical regions. Anthropogenic impacts such as land-use changes, habitat loss, and agriculture expansion can be directly associated with historical alterations in the ecology of birds, which can be observed through δ13C and δ15N values (Mason et al. 2020Mason NA, Unitt P, Sparks JP (2020) Agriculture induces isotopic shifts and niche contraction in Horned Larks (Eremophila alpestris) of the Colorado Desert. Journal of Ornithology 162: 381-393. https://doi.org/10.1007/s10336-020-01834-0
https://doi.org/10.1007/s10336-020-01834...
, Navarro et al. 2021aNavarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, Luz DTA, Silva WR, Pizo MA, Oliveira VC, Ferraz KMPMB (2021a) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130(11): 1892-1904. https://doi.org/10.1111/oik.08386
https://doi.org/10.1111/oik.08386...
). Navarro et al. (2021aNavarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, Luz DTA, Silva WR, Pizo MA, Oliveira VC, Ferraz KMPMB (2021a) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130(11): 1892-1904. https://doi.org/10.1111/oik.08386
https://doi.org/10.1111/oik.08386...
) showed that over 100 years of human expansion in a region of southeastern Brazil, the isotopic niche width of several trophic guilds (frugivores, granivores, insectivores, nectarivores, and omnivores) have been drastically reduced. Mason et al. (2020Mason NA, Unitt P, Sparks JP (2020) Agriculture induces isotopic shifts and niche contraction in Horned Larks (Eremophila alpestris) of the Colorado Desert. Journal of Ornithology 162: 381-393. https://doi.org/10.1007/s10336-020-01834-0
https://doi.org/10.1007/s10336-020-01834...
) also observed the narrowing of the niche of Eremophila alpestris (Linnaeus, 1758) since 1916, that is a widespread species in the northern hemisphere. Both studies suggest that the agricultural expansion in the study areas has decreased the amount and availability of food for these birds, consequently affecting their niche width. Given the severe land-use changes that can be observed in the Brazilian territory since the European colonization and markedly during the last hundred years, the use of isotopic analysis with museum specimens is important to understand the modifications in the ecology of tropical birds.

The human impact on the isotopic values of birds has also been addressed in ecological studies. For instance, changes in the δ15N values of birds may reflect an increased use of fertilizers in agriculture, or even an increase in garbage disposal (Blight et al. 2015Blight LK, Hobson KA, Kyser TK, Arcese P (2015) Changing gull diet in a changing world: A 150-year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America. Global Change Biology 21(4): 1497-1507. https://doi.org/10.1111/gcb.12796
https://doi.org/10.1111/gcb.12796...
, Møller et al. 2018Møller AP, Laursen K, Hobson KA (2018) Retrospectively analysing condition in historical samples of birds. Journal of Zoology 305(3): 188-195. https://doi.org/10.1111/jzo.12551
https://doi.org/10.1111/jzo.12551...
, Navarro et al. 2021aNavarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, Luz DTA, Silva WR, Pizo MA, Oliveira VC, Ferraz KMPMB (2021a) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130(11): 1892-1904. https://doi.org/10.1111/oik.08386
https://doi.org/10.1111/oik.08386...
). Navarro et al. (2021aNavarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, Luz DTA, Silva WR, Pizo MA, Oliveira VC, Ferraz KMPMB (2021a) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130(11): 1892-1904. https://doi.org/10.1111/oik.08386
https://doi.org/10.1111/oik.08386...
) discussed the reduction in δ15N values between historical and modern birds of different trophic guilds and its possible relationship with the increased use of synthetic nitrogen fertilizers in Brazil. Møller et al. (2018Møller AP, Laursen K, Hobson KA (2018) Retrospectively analysing condition in historical samples of birds. Journal of Zoology 305(3): 188-195. https://doi.org/10.1111/jzo.12551
https://doi.org/10.1111/jzo.12551...
) also showed the association among changes in δ15N values in contemporary birds, increased use of fertilizers in agriculture, and their negative consequences in the health of the feathers of Somateria mollissima (Linnaeus, 1758) in Denmark. Brazilian lands are known worldwide for their agricultural productivity and consequent negative influence on biodiversity (Moraes et al. 2017Moraes MCP, Mello K, Toppa RH (2017) Protected areas and agricultural expansion: Biodiversity conservation versus economic growth in the Southeast of Brazil. Journal of Environmental Management 188: 73-84. https://doi.org/10.1016/j.jenvman.2016.11.075
https://doi.org/10.1016/j.jenvman.2016.1...
). Notwithstanding, we still lack information on the influence of nitrogen fertilizers applied in landscapes on the morphological characteristics of native bird species.

Stable isotopes also allow us to ascertain changes in the migratory and geographic patterns of birds over time (e.g., Hobson et al. 2010Hobson KA, Greenberg R, Van Wilgenburg SL, Mettke-Hofmann C (2010) Migratory Connectivity in the Rusty Blackbird: Isotopic Evidence From Feathers of Historical and Contemporary Specimens. Condor 112(4): 778-788. https://doi.org/10.1525/cond.2010.100146
https://doi.org/10.1525/cond.2010.100146...
, Jiguet et al. 2020Jiguet F, Kardynal KJ, Hobson KA (2020) Feather stable isotope (δ2H) measurements suggest no historical variation in latitudinal origin of migrants in two declining songbirds. Journal of Ornithology 161(4): 1045-1050. https://doi.org/10.1007/s10336-020-01797-2
https://doi.org/10.1007/s10336-020-01797...
). Hobson et al. (2010Hobson KA, Greenberg R, Van Wilgenburg SL, Mettke-Hofmann C (2010) Migratory Connectivity in the Rusty Blackbird: Isotopic Evidence From Feathers of Historical and Contemporary Specimens. Condor 112(4): 778-788. https://doi.org/10.1525/cond.2010.100146
https://doi.org/10.1525/cond.2010.100146...
) evaluated whether historical and contemporary individuals of Euphagus carolinus (Statius Muller, 1776), a North American migratory species, have altered their geographic patterns since the nineteenth century. The results of δ2H indicate that the small changes in the eastern populations may result from changes in the quality and availability of habitat and food resources, which generated a valuable direction in conservation strategies for this bird (Hobson et al. 2010Hobson KA, Greenberg R, Van Wilgenburg SL, Mettke-Hofmann C (2010) Migratory Connectivity in the Rusty Blackbird: Isotopic Evidence From Feathers of Historical and Contemporary Specimens. Condor 112(4): 778-788. https://doi.org/10.1525/cond.2010.100146
https://doi.org/10.1525/cond.2010.100146...
). Jiguet et al. (2020Jiguet F, Kardynal KJ, Hobson KA (2020) Feather stable isotope (δ2H) measurements suggest no historical variation in latitudinal origin of migrants in two declining songbirds. Journal of Ornithology 161(4): 1045-1050. https://doi.org/10.1007/s10336-020-01797-2
https://doi.org/10.1007/s10336-020-01797...
) also found no geographical changes over the last 160 years for two declining migrant species in Europe, but argued that similar δ2H patterns between historical and modern individuals may result from a homogeneous latitudinal decrease in the populations of these birds. In Brazil, there is a diversity of migratory species that may be struggling against the negative effects of climate change on their movement patterns. The application of isotopic analysis can be a useful tool to understand these spatiotemporal changes.

Although long-term temporal studies are an expanding theme in bird ecology, some practical precautions in the use of isotopic analysis must be employed for the correct interpretation of the results. A representative sampling of the environmental isotopic baseline is essential in dietary studies, since it can represent a bias if it is not well addressed with adequate values that reflect the resources used in the time scale analyzed (Casey and Post 2011Casey MM, Post DM (2011) The problem of isotopic baseline: Reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106(1-2): 131-148. https://doi.org/10.1016/j.earscirev.2011.02.001
https://doi.org/10.1016/j.earscirev.2011...
). In this situation, natural history museum collections and herbariums are a significant source of food resource samples from the past, contributing to build an isotopic baseline. Another relevant precaution is the need to correct for isotopic values following temporal variations in the isotopic constitution of ecosystems and the atmosphere. The Suess effect represents a change in δ13C values in the atmosphere over the years, as a result of an increase in CO2 from anthropogenic activities (Revelle and Suess 1957Revelle R, Suess HE (1957) Carbon dioxide exchange between atmosphere and ocean and the question of an increase of atmospheric CO2 during the past decades. Tellus 9(1): 18-27. https://doi.org/10.1111/j.2153-3490.1957.tb01849.x
https://doi.org/10.1111/j.2153-3490.1957...
), and it should be considered in studies that aim to analyze historical biological data (Dombrosky 2020Dombrosky J (2020) A ~1000-year 13C Suess correction model for the study of past ecosystems. The Holocene 30(3): 474-478. https://doi.org/10.1177/0959683619887416
https://doi.org/10.1177/0959683619887416...
).

Protocol for feather collection in field samplings

The use of mist-nets in ecological studies to capture birds is common across Brazil. The Brazilian government agency responsible for standardizing the bird ringing process (CEMAVE/ICMBio) has already counted approximately one million individuals banded since 1977 (Sousa and Pereira 2020Sousa AEBA, Pereira PS (2020) Manual de anilhamento de aves silvestres. ICMBio-CEMAVE, Brasília, Brazil, 113 pp.). Despite the numerous projects involving bird capture, few efforts have been made to consolidate a feather collection protocol for isotopic analysis (Smith et al. 2003Smith TB, Marra PP, Webster MS, Lovette I, Gibbs HL, Holmes RT, Hobson KA, Rohwer S (2003) A call for feather sampling. Auk 120(1): 218-221. https://doi.org/10.2307/4090162
https://doi.org/10.2307/4090162...
). The rewards of building a solid isotopic database are enormous, as discussed elsewhere in this text.

Feathers are the most recommended tissue among ornithologists to build a comprehensive collection, since they are easy to collect and to store, and it is also an inert tissue for isotopic analysis (Smith et al. 2003Smith TB, Marra PP, Webster MS, Lovette I, Gibbs HL, Holmes RT, Hobson KA, Rohwer S (2003) A call for feather sampling. Auk 120(1): 218-221. https://doi.org/10.2307/4090162
https://doi.org/10.2307/4090162...
, Rutkowska et al. 2018Rutkowska M, Płotka-Wasylka J, Lubinska-Szczygeł M, Różańska A, Możejko-Ciesielska J, Namieśnik J (2018) Birds’ feathers - Suitable samples for determination of environmental pollutants. Trends in Analytical Chemistry 109: 97-115. https://doi.org/10.1016/j.trac.2018.09.022
https://doi.org/10.1016/j.trac.2018.09.0...
). More than one type of feather should be collected (primaries, rectrices, and breast contour), since the isotopic values between them may vary according to their molting period (Grecian et al. 2015Grecian WJ, McGill RAR, Phillips RA, Ryan PG, Furness RW (2015) Quantifying variation in δ13C and δ15N isotopes within and between feathers and individuals: Is one sample enough? Marine Biology 162(4): 733-741. https://doi.org/10.1007/s00227-015-2618-8
https://doi.org/10.1007/s00227-015-2618-...
). Multi-feather collection is also important in the case of migratory species, since the molting period may be correlated with the environmental aspects and geographic origin of the individuals (Costa et al. 2021Costa FJV, Hobson KA, Wunder MB, Nardoto GB (2021) Linking environmental indicators to blood, feather and claw δ18O in the Saffron Finch (Sicalis flaveola) in the central Brazilian savannas. Journal of Ornithology 163: 223-234. https://doi.org/10.1007/s10336-021-01939-0
https://doi.org/10.1007/s10336-021-01939...
). Collecting other tissues (e.g., blood, claw) is also relevant, since it can complement information on a temporal scale within the same individual. In this case, researchers must be trained specialists and comply with the ethics committees and animal welfare laws.

Besides tissue samples, some additional information is needed to build a strong database for the interpretation of isotopic data (Smith et al. 2003Smith TB, Marra PP, Webster MS, Lovette I, Gibbs HL, Holmes RT, Hobson KA, Rohwer S (2003) A call for feather sampling. Auk 120(1): 218-221. https://doi.org/10.2307/4090162
https://doi.org/10.2307/4090162...
). Researchers should identify each bird to the lowest possible taxonomic level, annotate the exact collecting location (geographic coordinates are preferable), and the date of collection (day, month, and year). Whenever possible, ornithologists should accurately report the sex and age of the individuals sampled. The food resources (e.g., invertebrates, fruits, seeds, flowers) available in the environment are valuable to compose the isotopic baseline, so it is important to emphasize the relevance of collecting some items by opportunistic search or through gut contents expelled by birds during the capture (e.g., regurgitates or feces). Food resources should preferably be stored dry or frozen, without chemical preservation methods (e.g., ethanol, formaldehyde), since preserving invertebrates in ethanol may alter their isotopic values (Jesus et al. 2015Jesus FM, Pereira MR, Rosa CS, Moreira MZ, Sperber CF (2015) Preservation methods alter carbon and nitrogen stable isotope values in crickets (Orthoptera: Grylloidea). PLoS One 10(9): e0137650. https://doi.org/10.1371/journal.pone.0137650
https://doi.org/10.1371/journal.pone.013...
). The recommendation for a widespread feather collection should not inhibit the traditional collection of museum specimens, but serve the purpose of increasing the availability of samples for isotopic and molecular analyses (Smith et al. 2003, Rocque and Winker 2005Rocque DA, Winker K (2005) Use of Bird Collections in Contaminant and Stable-Isotope Studies. Auk 122(3): 990-994.). The AviSample Network metadata repository is a global initiative that provides an opportunity for ornithologists to share all the information related to stored tissue samples, contributing for new collaborations among researchers and the reuse of avian samples (Brlík et al. 2022Brlík V, Pipek P, Brandis K, Chernetsov N, Costa FJV, Herrera LG, Kiat Y, Lanctot RB, Marra PP, Norris DR, Nwaogu CJ, Quillfeldt P, Saalfeld ST, Stricker CA, Thomson RL, Zhao T, Procházka P (2022) The reuse of avian samples: opportunities, pitfalls, and a solution. Ibis 164(1): 343-349. https://doi.org/10.1111/ibi.12997
https://doi.org/10.1111/ibi.12997...
).

The role of Brazilian museums in providing data and tissue samples

Natural History Museums are rich repositories of data that have been traditionally employed in studies of taxonomy and systematics. More recently, collections have been also used in ecological studies, including studies in isotopic ecology (Rocque and Winker 2005Rocque DA, Winker K (2005) Use of Bird Collections in Contaminant and Stable-Isotope Studies. Auk 122(3): 990-994., Wiley et al. 2017Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109.). Up to twenty years ago, the worldwide use of isotopic analysis in museum bird specimens was not common. In Brazil, ecological studies using this approach are even more recent and under-explored (Navarro et al. 2021aNavarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, Luz DTA, Silva WR, Pizo MA, Oliveira VC, Ferraz KMPMB (2021a) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130(11): 1892-1904. https://doi.org/10.1111/oik.08386
https://doi.org/10.1111/oik.08386...
). Brazilian museums, particularly the following three examples holding vast Neotropical bird collections, have enormous potential for stable isotope research: Museu de Zoologia da Universidade de São Paulo, Museu Paraense Emílio Goeldi, and Museu Nacional - UFRJ. Additionally, other museums and private collections throughout Brazil may prove valuable.

Despite the recent efforts to employ the isotopic tool and the accessibility of ornithological collections to molecular analyzes, there is still a need for greater interaction between Brazilian museum curators and isotopic ornithological research. One concern that may worry curators is the destruction of tissues from specimens (mainly feathers). Nevertheless, most studies require a small amount of feather sample (e.g., 1 mg or 0.5 cm²) to accurately analyze stable isotopes, and this does not visually alter the specimen (Wiley et al. 2017Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109.). A small piece of sample is sufficient to bring relevant results to understand the ecology of endangered species and assist in planning the conservation of target birds (Tawa and Sagawa 2021Tawa K, Sagawa S (2021) Stable isotopic analysis of stuffed specimens revealed the feeding habits of Oriental Storks Ciconia boyciana in Japan before their extinction in the wild. Journal of Ornithology 162: 193-206. https://doi.org/10.1007/s10336-020-01806-4
https://doi.org/10.1007/s10336-020-01806...
). Another point to be considered, is the creation of an integrated open access database of bird isotopic values, which will help to avoid the re-sampling of feathers and other tissues from species in museums and collections that have already been sampled. Besides that, this initiative would also stimulate scientific partnership among researchers to explore other aspects of a species’ ecology or to provide complementary information to other analytical methods.

Improving tools to assist forensics and illegal bird trade

Isotopic analysis can also be employed in forensic studies to help determine the geographic origin of seized birds (Nardoto et al. 2017Nardoto GB, Ribeiro JF, Sena-Souza JP, Guaraldo AC, Saquetti CH (2017) rastreamento forense: uso dos isótopos estáveis no combate ao crime. In: Costa FJV, Ferreira JM, Monteiro KRG, Mayrink RR (Eds) Ciência contra o tráfico: Avanços no combate ao comércio ilegal de animais silvestres. Imprell Gráfica e Editora, João Pessoa, 51-78., Andersson et al. 2021Andersson AA, Gibson L, Baker DM, Cybulski JD, Wang S, Leung B, Chu LM, Dingle C (2021) Stable isotope analysis as a tool to detect illegal trade in critically endangered cockatoos. Animal Conservation 24(6): 1021-1031. https://doi.org/10.1111/acv.12705
https://doi.org/10.1111/acv.12705...
). In Brazil, besides the impacts of fragmentation and habitat loss, the illegal trade of species is one of the major threats to bird diversity (Marini and Garcia 2005Marini MÂ, Garcia FI (2005) Bird Conservation in Brazil. Conservation Biology 19(3): 665-671.). Approximately 23% of Brazilian bird species are traded illegally, many of which are classified into threatened categories of IUCN (Alves et al. 2013Alves RRN, Lima JRF, Araujo HFP (2013) The live bird trade in Brazil and its conservation implications: an overview. Bird Conservation International 23(1): 53-65. https://doi.org/10.1017/S095927091200010X
https://doi.org/10.1017/S095927091200010...
). Associating isoscapes and isotopic values of seized individuals may be useful to determine trafficking routes in Brazil, and target more effective strategies to fight against illegal bird trade (Sena-Souza et al. 2019Sena-Souza JP, Costa FJV, Nardoto GB (2019) Background and the use of isoscapes in the Brazilian context: essential tool for isotope data interpretation and natural resource management. Ambiente e Agua - An Interdisciplinary Journal of Applied Science 14(2): 1. https://doi.org/10.4136/ambi-agua.2282
https://doi.org/10.4136/ambi-agua.2282...
). Additionally, the release of seized and recovered birds in unsuitable locations (outside their geographic range) may pose a potential risk to wild populations (Marini and Garcia 2005Marini MÂ, Garcia FI (2005) Bird Conservation in Brazil. Conservation Biology 19(3): 665-671., Efe et al. 2006Efe MA, Martins-Ferreira C, Olmos F, Mohr LV, Silveira LF (2006) Diretrizes da Sociedade Brasileira de Ornitologia para a destinação de aves silvestres provenientes do tráfico e cativeiro. Revista Brasileira de Ornitologia 14(1): 67-72.). Thus, isotopic analysis can be a relevant tool to identify the origin of individuals and establish appropriate places for their release.

The continuous generation of isoscapes for the Brazilian territory will increase the robustness of isotopic analysis in forensics. Efforts are already being implemented to understand the isotopic differences among distinct vegetation types and precipitation patterns in the Brazilian biomes (e.g., Gastmans et al. 2017Gastmans D, Santos V, Galhardi JA, Gromboni JF, Batista LV, Miotlinski K, Chang HK, Govone JS (2017) Controls over spatial and seasonal variations on isotopic composition of the precipitation along the central and eastern portion of Brazil. Isotopes in Environmental and Health Studies 53(5): 518-538. https://doi.org/10.1080/10256016.2017.1305376
https://doi.org/10.1080/10256016.2017.13...
, Martinelli et al. 2020Martinelli LA, Nardoto GB, Soltangheisi A, Reis CRG, Abdalla-Filho AL, Camargo PB, Domingues TF, Faria D, Figueira AM, Gomes TF, Lins SRM, Mardegan SF, Mariano E, Miatto RC, Moraes R, Moreira MZ, Oliveira RS, Ometto JPHB, Santos FLS, Sena-Souza J, Silva DML, Silva JCSS, Vieira SA (2020) Determining ecosystem functioning in Brazilian biomes through foliar carbon and nitrogen concentrations and stable isotope ratios. Biogeochemistry 117(43): 26842-26848. https://doi.org/10.1007/s10533-020-00714-2
https://doi.org/10.1007/s10533-020-00714...
). Expanding these efforts may help to fight against the illegal trade of wildlife, such as increasing coverage from the Global Network of Isotopes in Precipitation (GNIP), which provides data on temporal and spatial variations of environmental isotopes in precipitation. Another important process that should be better understood to improve the stable isotope tool in forensics is the molting periods of distinct bird taxa, promoting the correct interpretation of individual isotopic values and geographic origin. More recently, the use of compound-specific isotope analysis (CSIA) has gained interest. It consists of obtaining the isotopic value of amino acids rather than of bulk tissues (Ishikawa 2018Ishikawa NF (2018) Use of compound-specific nitrogen isotope analysis of amino acids in trophic ecology: assumptions, applications, and implications. Ecological Research 33(5): 825-837. https://doi.org/10.1007/s11284-018-1616-y
https://doi.org/10.1007/s11284-018-1616-...
). Since essential amino acids do not undergo biochemical reactions, their isotopic values directly reflect the food ingested and isotopic data from diet sources are not necessary (Whiteman et al. 2019Whiteman J, Elliott Smith E, Besser A, Newsome S (2019) A Guide to Using Compound-Specific Stable Isotope Analysis to Study the Fates of Molecules in Organisms and Ecosystems. Diversity 11(1): 8. https://doi.org/10.3390/d11010008
https://doi.org/10.3390/d11010008...
). This recent advance promises more accurate and informative isotopic values, helping to improve the forensic tool used to fight illegal bird trade (Andersson et al. 2021Andersson AA, Gibson L, Baker DM, Cybulski JD, Wang S, Leung B, Chu LM, Dingle C (2021) Stable isotope analysis as a tool to detect illegal trade in critically endangered cockatoos. Animal Conservation 24(6): 1021-1031. https://doi.org/10.1111/acv.12705
https://doi.org/10.1111/acv.12705...
).

Financial and sample size shortcomings

Despite the advantages of using stable isotopes as a tool to understand the ecology of species, there is still a financial constraint that prevents researchers from considering this method. The analysis can cost $10-20 US dollars per sample, depending on the number of isotopes of interest and whether the researcher already sends the samples prepared for the analysis, or not. If the samples are sent for analysis outside of Brazil, there are additional shipping costs and the samples must be registered with the SISGEN system (Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado). The cost of an isotopic study depends on the total number of samples analyzed, which may vary according to objectives of the research. Ecological studies usually use the rule of thumb to determine a reliable sample size (n = 30), but this should not be unconditional, since the experimental design must follow the assumptions of the analyzes employed (Martínez-Abraín 2014Martínez-Abraín A (2014) Is the “n = 30 rule of thumb” of ecological field studies reliable? A call for greater attention to the variability in our data. Animal Biodiversity and Conservation 37(1): 95-100.). Some isotopic niche analyzes suggest a minimum of 10-15 samples per group, to obtain consistent and robust results (Jackson et al. 2011Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80(3): 595-602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
https://doi.org/10.1111/j.1365-2656.2011...
, Eckrich et al. 2020Eckrich CA, Albeke SE, Flaherty EA, Bowyer RT, Ben-David M (2020) rKIN: Kernel-based method for estimating isotopic niche size and overlap. Journal of Animal Ecology 89(3): 757-771. https://doi.org/10.1111/1365-2656.13159
https://doi.org/10.1111/1365-2656.13159...
) although studies with other approaches may require more samples. It is relevant to point out that using conventional methodologies is not necessarily cheaper, as it requires greater field effort and the acquisition of other tools to achieve the same results obtained with stable isotopes. Even so, although isotopic analysis is not expensive, it is not yet widely available nor is it under consideration by Brazilian researchers when designing new project funding proposals. Additionally, it is desirable to establish collaboration between researchers in ornithology and isotopic ecology, increasing the analytical power of the study.

Final remarks

The Brazilian scenario for exploring the isotopic analysis of terrestrial birds is promising. There are many ecological topics that can be approached with this tool. Even the most common stable isotopes in ecology studies (carbon, nitrogen, hydrogen, and oxygen) are still not frequently used in studies originating in Brazil. Trophic ecology is one topic that may benefit from the use of isotopic analysis, since it provides robust information about the diet, use of habitat, and species’ niche (e.g., Kelly 2000Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78(1): 1-27., Newsome et al. 2007Newsome SD, Martínez del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5(8): 429-436. https://doi.org/10.1890/060150.01
https://doi.org/10.1890/060150.01...
, Boecklen et al. 2011Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics 42: 411-440. https://doi.org/10.1146/annurev-ecolsys-102209-144726
https://doi.org/10.1146/annurev-ecolsys-...
). Detecting the migratory and geographic patterns of birds is another interesting topic to be addressed with stable isotopes (e.g., Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
, Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
), especially in a territory where there is great diversity of migratory species. Studies on physiology and laboratory experiments are crucial to improve the isotopic method, adapting it to the reality of native species (e.g., Martínez del Rio et al. 2009bMartínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009b) Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84: 91-111. https://doi.org/10.1111/j.1469-185X.2008.00064.x
https://doi.org/10.1111/j.1469-185X.2008...
, Hobson 2011Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
https://doi.org/10.1007/s10336-011-0653-...
). Additionally, valuing museums and ornithological collections may promote desirable opportunities to increase our knowledge about the ecological history of birds and to compare it with the contemporary ecology, to help devise conservation strategies (e.g., Wiley et al. 2017Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109.).

Despite so many opportunities for studies in the Brazilian territory using stable isotopes and birds, there are still some challenges to be considered before the enthusiasm for the tool grows. Researchers interested in employing isotopic analysis must know the methodological shortcomings to correctly interpret the results (Inger and Bearhop 2008Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
https://doi.org/10.1111/j.1474-919X.2008...
, Caut et al. 2009Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): The effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46(2): 443-453. https://doi.org/10.1111/j.1365-2664.2009.01620.x
https://doi.org/10.1111/j.1365-2664.2009...
, Casey and Post 2011Casey MM, Post DM (2011) The problem of isotopic baseline: Reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106(1-2): 131-148. https://doi.org/10.1016/j.earscirev.2011.02.001
https://doi.org/10.1016/j.earscirev.2011...
). If precautions are taken, however, the benefits of using isotopes to broaden our knowledge of bird ecology will become increasingly evident. In a country with such a vast territory, composed of six biomes, all under intense pressure from anthropogenic impacts (land-use changes, habitat loss, fragmentation), the use of isotopic analysis in new ornithological studies is promising.

ACKNOWLEDGEMENTS

ABN thanks the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the doctoral scholarship (process 2020/07619-0) and LFS thanks the Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico (CNPq) for the research grant (CNPq 302291/2016-6 and 308337/2019-0) and to the Fundação de Amparo à Pesquisa do Estado de São Paulo to the ARCA project (Thematic project FAPESP, 2017/23548-2). We also thank the reviewers for their valuable comments and contributions.

LITERATURE CITED

  • Alves RRN, Lima JRF, Araujo HFP (2013) The live bird trade in Brazil and its conservation implications: an overview. Bird Conservation International 23(1): 53-65. https://doi.org/10.1017/S095927091200010X
    » https://doi.org/10.1017/S095927091200010X
  • Andersson AA, Gibson L, Baker DM, Cybulski JD, Wang S, Leung B, Chu LM, Dingle C (2021) Stable isotope analysis as a tool to detect illegal trade in critically endangered cockatoos. Animal Conservation 24(6): 1021-1031. https://doi.org/10.1111/acv.12705
    » https://doi.org/10.1111/acv.12705
  • Araújo MS, Bolnick DI, Machado G, Giaretta AA, Reis SF (2007) Using δ13C Stable Isotopes to Quantify Individual-Level Diet Variation. Oecologia 152(4): 643-654. https://doi.org/10.1007/s00442-007-0687-l
    » https://doi.org/10.1007/s00442-007-0687-l
  • Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecology Letters 14(9): 948-958. https://doi.org/10.1111/j.1461-0248.2011.01662.x
    » https://doi.org/10.1111/j.1461-0248.2011.01662.x
  • Atkinson PW, Baker AJ, Bevan RM, Clark NA, Cole KB, Gonzalez PM, Newton J, Niles LJ, Robinson RA (2005) Unravelling the migration and moult strategies of a long-distance migrant using stable isotopes: Red Knot Calidris canutus movements in the Americas. Ibis 147(4): 738-749. https://doi.org/10.1111/j.1474-919x.2005.00455.x
    » https://doi.org/10.1111/j.1474-919x.2005.00455.x
  • Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors That Influence Assimilation Rates and Fractionation of Nitrogen and Carbon Stable Isotopes in Avian Blood and Feathers. Physiological and Biochemical Zoology 75(5): 451-458. https://doi.org/10.1086/342800
    » https://doi.org/10.1086/342800
  • Bearhop S, Furness RW, Hilton GM, Votier SC, Waldron S (2003) A forensic approach to understanding diet and habitat use from stable isotope analysis of (avian) claw material. Functional Ecology 17(2): 270-275. https://doi.org/10.1046/j.1365-2435.2003.00725.x
    » https://doi.org/10.1046/j.1365-2435.2003.00725.x
  • Ben-David M, Flaherty EA (2012) Stable isotopes in mammalian research: a beginner’s guide. Journal of Mammalogy 93(2): 312-328. https://doi.org/10.1644/11-mamm-s-166.1
    » https://doi.org/10.1644/11-mamm-s-166.1
  • Blight LK, Hobson KA, Kyser TK, Arcese P (2015) Changing gull diet in a changing world: A 150-year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America. Global Change Biology 21(4): 1497-1507. https://doi.org/10.1111/gcb.12796
    » https://doi.org/10.1111/gcb.12796
  • Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics 42: 411-440. https://doi.org/10.1146/annurev-ecolsys-102209-144726
    » https://doi.org/10.1146/annurev-ecolsys-102209-144726
  • Boesing AL, Marques TS, Martinelli LA, Nichols E, Siqueira PR, Beier C, Camargo PB, Metzger JP (2021) Conservation implications of a limited avian cross-habitat spillover in pasture lands. Biological Conservation 253: 108898. https://doi.org/10.1016/j.biocon.2020.108898
    » https://doi.org/10.1016/j.biocon.2020.108898
  • Bond AL, Hobson KA (2012) Reporting stable-isotope ratios in ecology: recommended terminology, guidelines and best practices. Waterbirds 35(2): 324. https://doi.org/10.1675/063.035.0213
    » https://doi.org/10.1675/063.035.0213
  • Bond AL, Jardine TD, Hobson KA (2016) Multi-tissue stable-isotope analyses can identify dietary specialization. Methods in Ecology and Evolution 7(12): 1428-1437. https://doi.org/10.1111/2041-210X.12620
    » https://doi.org/10.1111/2041-210X.12620
  • Bosenbecker C, Bugoni L (2020) Trophic niche similarities of sympatric Turdus thrushes determined by fecal contents, stable isotopes, and bipartite network approaches. Ecology and Evolution 10(17): 9073-9084. https://doi.org/10.1002/ece3.6485
    » https://doi.org/10.1002/ece3.6485
  • Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143(3): 337-348. https://doi.org/10.1007/s00442-004-1813-y
    » https://doi.org/10.1007/s00442-004-1813-y
  • Brlík V, Pipek P, Brandis K, Chernetsov N, Costa FJV, Herrera LG, Kiat Y, Lanctot RB, Marra PP, Norris DR, Nwaogu CJ, Quillfeldt P, Saalfeld ST, Stricker CA, Thomson RL, Zhao T, Procházka P (2022) The reuse of avian samples: opportunities, pitfalls, and a solution. Ibis 164(1): 343-349. https://doi.org/10.1111/ibi.12997
    » https://doi.org/10.1111/ibi.12997
  • Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Communications in Mass Spectrometry 22(16): 2457-2462. https://doi.org/10.1002/rcm.3633
    » https://doi.org/10.1002/rcm.3633
  • Cardenas-Ortiz L, Bayly NJ, Kardynal KJ, Hobson KA (2020) Defining catchment origins of a geographical bottleneck: Implications of population mixing and phenological overlap for the conservation of Neotropical migratory birds. Condor 122(2): duaa004. https://doi.org/10.1093/condor/duaa004
    » https://doi.org/10.1093/condor/duaa004
  • Caron-Beaudoin É, Gentes ML, Patenaude-Monette M, Hélie JF, Giroux JF, Verreault J (2013) Combined usage of stable isotopes and GPS-based telemetry to understand the feeding ecology of an omnivorous bird, the Ring-billed Gull (Larus delawarensis). Canadian Journal of Zoology 91(10): 689-697.
  • Carvalho FMV, De Marco P, Ferreira LG (2009) The Cerrado into-pieces: Habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biological Conservation 142(7): 1392-1403. https://doi.org/10.1016/j.biocon.2009.01.031
    » https://doi.org/10.1016/j.biocon.2009.01.031
  • Casey MM, Post DM (2011) The problem of isotopic baseline: Reconstructing the diet and trophic position of fossil animals. Earth-Science Reviews 106(1-2): 131-148. https://doi.org/10.1016/j.earscirev.2011.02.001
    » https://doi.org/10.1016/j.earscirev.2011.02.001
  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): The effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46(2): 443-453. https://doi.org/10.1111/j.1365-2664.2009.01620.x
    » https://doi.org/10.1111/j.1365-2664.2009.01620.x
  • Cheesman AW, Cernusak LA (2016) Isoscapes: A new dimension in community ecology. Tree Physiology 36(12): 1456-1459. https://doi.org/10.1093/treephys/tpw099
    » https://doi.org/10.1093/treephys/tpw099
  • Chesson LA, Barnette JE, Bowen GJ, Brooks JR, Casale JF, Cerling TE, Cook CS, Douthitt CB, Howa JD, Hurley JM, Kreuzer HW, Lott MJ, Martinelli LA, O’Grady SP, Podlesak DW, Tipple BJ, Valenzuela LO, West JB (2018) Applying the principles of isotope analysis in plant and animal ecology to forensic science in the Americas. Oecologia 187: 1077-1094. https://doi.org/10.1007/s00442-018-4188-1
    » https://doi.org/10.1007/s00442-018-4188-1
  • Costa FJV, Hobson KA, Wunder MB, Nardoto GB (2021) Linking environmental indicators to blood, feather and claw δ18O in the Saffron Finch (Sicalis flaveola) in the central Brazilian savannas. Journal of Ornithology 163: 223-234. https://doi.org/10.1007/s10336-021-01939-0
    » https://doi.org/10.1007/s10336-021-01939-0
  • DeNiro MJ, Epstein S (1976) You are what you eat (plus a few ‰): the carbon isotope cycle in food chains. Geological Society of America 6: 834.
  • Dodds WK, Collins SM, Hamilton SK, Tank JL, Johnson S, Webster JR, Simon KS, Whiles MR, Rantala HM, McDowell WH, Peterson SD, Riis T, Crenshaw CL, Thomas SA, Kristensen PB, Cheever BM, Flecker AS, Griffiths NA, Crowl T, Rosi-Marshall EJ, El-Sabaawi R, Martí E (2014) You are not always what we think you eat: selective assimilation across multiple whole-stream isotopic tracer studies. Ecology 95(10): 2757-2767. https://doi.org/10.1890/13-2276.1
    » https://doi.org/10.1890/13-2276.1
  • Dombrosky J (2020) A ~1000-year 13C Suess correction model for the study of past ecosystems. The Holocene 30(3): 474-478. https://doi.org/10.1177/0959683619887416
    » https://doi.org/10.1177/0959683619887416
  • Durães R, Marini MAÂ (2005) A quantitative assessment of bird diets in the Brazilian Atlantic Forest, with recommendations for future diet studies. Ornitología Neotropical 16: 65-83.
  • Eckrich CA, Albeke SE, Flaherty EA, Bowyer RT, Ben-David M (2020) rKIN: Kernel-based method for estimating isotopic niche size and overlap. Journal of Animal Ecology 89(3): 757-771. https://doi.org/10.1111/1365-2656.13159
    » https://doi.org/10.1111/1365-2656.13159
  • Efe MA, Martins-Ferreira C, Olmos F, Mohr LV, Silveira LF (2006) Diretrizes da Sociedade Brasileira de Ornitologia para a destinação de aves silvestres provenientes do tráfico e cativeiro. Revista Brasileira de Ornitologia 14(1): 67-72.
  • English PA, Green DJ, Nocera JJ (2018) Stable isotopes from museum specimens may provide evidence of long-term change in the trophic ecology of a migratory aerial insectivore. Frontiers in Ecology and Evolution 6: 14. https://doi.org/10.3389/fevo.2018.00014
    » https://doi.org/10.3389/fevo.2018.00014
  • Ferger SW, Bohning-Gaese K, Wilcke W, Oelmann Y, Schleuning M (2013) Distinct carbon sources indicate strong differentiation between tropical forest and farmland bird communities. Oecologia 171: 473-486. https://doi.org/10.1007/s00442-012-2422-9
    » https://doi.org/10.1007/s00442-012-2422-9
  • Fox T, Bearhop S (2008) The use of stable-isotope ratios in ornithology. British Birds 101(3): 112-130.
  • Fry B (2008) Stable Isotope Ecology. Springer, New York, 316 pp.
  • Gastmans D, Santos V, Galhardi JA, Gromboni JF, Batista LV, Miotlinski K, Chang HK, Govone JS (2017) Controls over spatial and seasonal variations on isotopic composition of the precipitation along the central and eastern portion of Brazil. Isotopes in Environmental and Health Studies 53(5): 518-538. https://doi.org/10.1080/10256016.2017.1305376
    » https://doi.org/10.1080/10256016.2017.1305376
  • González-Carcacía JA, Gerardo Herrera LM, Nassar JM (2020) Dietary importance of C3 and CAM food pathways for birds in a Neotropical semiarid zone. Biotropica 52(5): 938-945. https://doi.org/10.1111/btp.12798
    » https://doi.org/10.1111/btp.12798
  • Graves GR, Newsome SD, Willard DE, Grosshuesch DA, Wurzel WW, Fogel ML (2012). Nutritional stress and body condition in the Great Gray Owl (Strix nebulosa) during winter irruptive migrations. Canadian Journal of Zoology 90(7): 787-797. https://doi.org/10.1139/z2012-047
    » https://doi.org/10.1139/z2012-047
  • Grecian WJ, McGill RAR, Phillips RA, Ryan PG, Furness RW (2015) Quantifying variation in δ13C and δ15N isotopes within and between feathers and individuals: Is one sample enough? Marine Biology 162(4): 733-741. https://doi.org/10.1007/s00227-015-2618-8
    » https://doi.org/10.1007/s00227-015-2618-8
  • Guaraldo AC, Kelly JF, Marini MÂ (2016) Contrasting annual cycles of an intratropical migrant and a tropical resident bird. Journal of Ornithology 157(3): 695-705. https://doi.org/10.1007/s10336-016-1327-5
    » https://doi.org/10.1007/s10336-016-1327-5
  • Guaraldo AC, Kelly JF, Marini MÂ (2019) Independent trophic behavior and breeding success of a resident flycatcher and a coexisting migratory congener. Austral Ecology 44(1): 126-137. https://doi.org/10.1111/aec.12660
    » https://doi.org/10.1111/aec.12660
  • Hardesty J (2009) Using nitrogen-15 to examine protein sources in hummingbird diets. Ornitología Colombiana 8: 19-28.
  • Healy K, Guillerme T, Kelly SBAA, Inger R, Bearhop S, Jackson AL (2018) SIDER: An R package for predicting trophic discrimination factors of consumers based on their ecology and phylogenetic relatedness. Ecography 41(8): 1393-1400. https://doi.org/10.1111/ecog.03371
    » https://doi.org/10.1111/ecog.03371
  • Hebert CE, Wassenaar LI (2001) Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. Environmental Science and Technology 35(17): 3482-3487. https://doi.org/10.1021/es001970p
    » https://doi.org/10.1021/es001970p
  • Herrera LG, Hobson KA, Rodríguez M, Hernandez P (2003) Trophic partitioning in tropical rain forest birds: insights from stable isotope analysis. Oecologia 136(3): 439-444. https://doi.org/10.1007/s00442-003-1293-5
    » https://doi.org/10.1007/s00442-003-1293-5
  • Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314-326.
  • Hobson KA (2011) Isotopic ornithology: A perspective. Journal of Ornithology 152: S49-S66. https://doi.org/10.1007/s10336-011-0653-x
    » https://doi.org/10.1007/s10336-011-0653-x
  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I : Turnover of 13C in tissues. Condor 94(1): 181-188.
  • Hobson KA, Norris DR (2008) Animal migration: a context for using new techniques and approaches. In: Hobson KA, Wassenaar LI (Eds) Tracking animal migration with stable isotopes. Academic Press, London, 1-19.
  • Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95(2): 388-394.
  • Hobson KA, Wassenaar LI, Milá B, Lovette I, Dingle C, Smith TB (2003) Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia 136: 302-308.
  • Hobson KA, Greenberg R, Van Wilgenburg SL, Mettke-Hofmann C (2010) Migratory Connectivity in the Rusty Blackbird: Isotopic Evidence From Feathers of Historical and Contemporary Specimens. Condor 112(4): 778-788. https://doi.org/10.1525/cond.2010.100146
    » https://doi.org/10.1525/cond.2010.100146
  • Hobson KA, Van Wilgenburg SL, Wassenaar LI, Powell RL, Still CJ, Craine JM (2012) A multi-isotope (δ13C, δ15N, δ2H) feather isoscape to assign Afrotropical migrant birds to origins. Ecosphere 3(5): 1-20. https://doi.org/10.1890/ES12-00018.1
    » https://doi.org/10.1890/ES12-00018.1
  • Hobson KA, Van Wilgenburg SL, Faaborg J, Toms JD, Rengifo C, Sosa AL, Aubry Y, Brito Aguilar R (2014) Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity. Journal of Field Ornithology 85(3): 237-257. https://doi.org/10.1111/jofo.12065
    » https://doi.org/10.1111/jofo.12065
  • Hobson KA, Wassenaar LI, Bowen GJ, Courtiol A, Trueman CN, Voigt CC, West JB, McMahon KW, Newsome SD (2019) Outlook for Using Stable Isotopes in Animal Migration Studies. In: Hobson KA, Wassenaar LI (Eds) Tracking animal migration with stable isotopes . Academic Press, London , 237-244.
  • Hopkins JB, Ferguson JM (2012) Estimating the diets of animals using stable isotopes and a comprehensive Bayesian mixing model. PLoS One 7(1): e28478. https://doi.org/10.1371/journal.pone.0028478
    » https://doi.org/10.1371/journal.pone.0028478
  • Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150: 447-461. https://doi.org/10.1111/j.1474-919X.2008.00839.x
    » https://doi.org/10.1111/j.1474-919X.2008.00839.x
  • Ishikawa NF (2018) Use of compound-specific nitrogen isotope analysis of amino acids in trophic ecology: assumptions, applications, and implications. Ecological Research 33(5): 825-837. https://doi.org/10.1007/s11284-018-1616-y
    » https://doi.org/10.1007/s11284-018-1616-y
  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80(3): 595-602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
    » https://doi.org/10.1111/j.1365-2656.2011.01806.x
  • Jesus FM, Pereira MR, Rosa CS, Moreira MZ, Sperber CF (2015) Preservation methods alter carbon and nitrogen stable isotope values in crickets (Orthoptera: Grylloidea). PLoS One 10(9): e0137650. https://doi.org/10.1371/journal.pone.0137650
    » https://doi.org/10.1371/journal.pone.0137650
  • Jiguet F, Kardynal KJ, Hobson KA (2020) Feather stable isotope (δ2H) measurements suggest no historical variation in latitudinal origin of migrants in two declining songbirds. Journal of Ornithology 161(4): 1045-1050. https://doi.org/10.1007/s10336-020-01797-2
    » https://doi.org/10.1007/s10336-020-01797-2
  • John Glew KS, Wanless S, Harris MP, Daunt F, Erikstad KE, Strøm H, Trueman CN (2018) Moult location and diet of auks in the north sea inferred from coupled light-based and isotope-based geolocation. Marine Ecology Progress Series 599: 239-251. https://doi.org/10.3354/meps12624
    » https://doi.org/10.3354/meps12624
  • Jovani R, Rohwer S (2017) Fault bars in bird feathers: mechanisms, and ecological and evolutionary causes and consequences. Biological Reviews 92(2): 1113-1127. https://doi.org/10.1111/brv.12273
    » https://doi.org/10.1111/brv.12273
  • Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Canadian Journal of Zoology 78(1): 1-27.
  • Kempster B, Zanette L, Longstaffe FJ, MacDougall-Shackleton SA, Wingfield JC, Clinchy M (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151(3): 365-371. https://doi.org/10.1007/s00442-006-0597-7
    » https://doi.org/10.1007/s00442-006-0597-7
  • Layman CA, Araújo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: An overview of analytical tools. Biological Reviews 87(3): 545-562. https://doi.org/10.1111/j.1469-185X.2011.00208.x
    » https://doi.org/10.1111/j.1469-185X.2011.00208.x
  • Lopes LE, Fernandes AM, Marini MÂ (2005) Diet of some Atlantic Forest birds. Ararajuba 13(1): 95-103.
  • Magioli M, Moreira MZ, Fonseca RCB, Ribeiro MC, Rodrigues MG, Ferraz KMPMB (2019) Human-modified landscapes alter mammal resource and habitat use and trophic structure. Proceedings of the National Academy of Sciences 116(37): 18466-18472. https://doi.org/10.1073/pnas.1904384116
    » https://doi.org/10.1073/pnas.1904384116
  • Magioli M, Ferraz KMPMB, Chiarello AG, Galetti M, Setz EZF, Paglia AP, Abrego N, Ribeiro MC, Ovaskainen O (2021) Land-use changes lead to functional loss of terrestrial mammals in a Neotropical rainforest. Perspectives in Ecology and Conservation 19(2): 161-170. https://doi.org/10.1016/j.pecon.2021.02.006
    » https://doi.org/10.1016/j.pecon.2021.02.006
  • Marini MÂ, Garcia FI (2005) Bird Conservation in Brazil. Conservation Biology 19(3): 665-671.
  • Martinelli LA, Ometto JPHB, Ferraz ES, Victoria RL, Camargo PB, Moreira MZ (2009) Desvendando questões ambientais com isótopos estáveis. Oficina de textos, São Paulo, 144 pp.
  • Martinelli LA, Nardoto GB, Soltangheisi A, Reis CRG, Abdalla-Filho AL, Camargo PB, Domingues TF, Faria D, Figueira AM, Gomes TF, Lins SRM, Mardegan SF, Mariano E, Miatto RC, Moraes R, Moreira MZ, Oliveira RS, Ometto JPHB, Santos FLS, Sena-Souza J, Silva DML, Silva JCSS, Vieira SA (2020) Determining ecosystem functioning in Brazilian biomes through foliar carbon and nitrogen concentrations and stable isotope ratios. Biogeochemistry 117(43): 26842-26848. https://doi.org/10.1007/s10533-020-00714-2
    » https://doi.org/10.1007/s10533-020-00714-2
  • Martínez-Abraín A (2014) Is the “n = 30 rule of thumb” of ecological field studies reliable? A call for greater attention to the variability in our data. Animal Biodiversity and Conservation 37(1): 95-100.
  • Martínez del Rio C, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009a) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161: 149-159. https://doi.org/10.1007/s00442-009-1357-2
    » https://doi.org/10.1007/s00442-009-1357-2
  • Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009b) Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84: 91-111. https://doi.org/10.1111/j.1469-185X.2008.00064.x
    » https://doi.org/10.1111/j.1469-185X.2008.00064.x
  • Mason NA, Unitt P, Sparks JP (2020) Agriculture induces isotopic shifts and niche contraction in Horned Larks (Eremophila alpestris) of the Colorado Desert. Journal of Ornithology 162: 381-393. https://doi.org/10.1007/s10336-020-01834-0
    » https://doi.org/10.1007/s10336-020-01834-0
  • McGill B, Enquist B, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21(4): 178-185. https://doi.org/10.1016/j.tree.2006.02.002
    » https://doi.org/10.1016/j.tree.2006.02.002
  • McKinnon EA, Kurt Kyser T, Stutchbury BJM (2017) Does the proportion of arthropods versus fruit in the diet influence overwintering condition of an omnivorous songbird? Journal of Field Ornithology 88(1): 65-79. https://doi.org/10.1111/jofo.12187
    » https://doi.org/10.1111/jofo.12187
  • Møller AP, Laursen K, Hobson KA (2018) Retrospectively analysing condition in historical samples of birds. Journal of Zoology 305(3): 188-195. https://doi.org/10.1111/jzo.12551
    » https://doi.org/10.1111/jzo.12551
  • Moraes MCP, Mello K, Toppa RH (2017) Protected areas and agricultural expansion: Biodiversity conservation versus economic growth in the Southeast of Brazil. Journal of Environmental Management 188: 73-84. https://doi.org/10.1016/j.jenvman.2016.11.075
    » https://doi.org/10.1016/j.jenvman.2016.11.075
  • Nardoto GB, Ribeiro JF, Sena-Souza JP, Guaraldo AC, Saquetti CH (2017) rastreamento forense: uso dos isótopos estáveis no combate ao crime. In: Costa FJV, Ferreira JM, Monteiro KRG, Mayrink RR (Eds) Ciência contra o tráfico: Avanços no combate ao comércio ilegal de animais silvestres. Imprell Gráfica e Editora, João Pessoa, 51-78.
  • Navarro AB, Magioli M, Bogoni JA, Silveira LF, Moreira MZ, Alexandrino ER, Luz DTA, Silva WR, Pizo MA, Oliveira VC, Ferraz KMPMB (2021a) Isotopic niches of tropical birds reduced by anthropogenic impacts: a 100-year perspective. Oikos 130(11): 1892-1904. https://doi.org/10.1111/oik.08386
    » https://doi.org/10.1111/oik.08386
  • Navarro AB, Magioli M, Bogoni JA, Moreira MZ, Silveira LF, Alexandrino ER, Luz DTA, Pizo MA, Silva WR, Oliveira VC, Donatelli RJ, Christianini AV, Piratelli AJ, Ferraz KMPMB (2021b) Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196: 171-184. https://doi.org/10.1007/s00442-021-04908-9
    » https://doi.org/10.1007/s00442-021-04908-9
  • Newsome SD, Martínez del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Frontiers in Ecology and the Environment 5(8): 429-436. https://doi.org/10.1890/060150.01
    » https://doi.org/10.1890/060150.01
  • Newsome SD, Sabat P, Wolf N, Rader JA, DelRio CM (2015) Multi-tissue δ2H analysis reveals altitudinal migration and tissue-specific discrimination patterns in Cinclodes. Ecosphere 6(11): 1-18.
  • Newton J (2016) Stable Isotopes as Tools inEcological Research. In: eLS Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, 1-8. https://doi.org/10.1002/9780470015902.a0021231.pub2
    » https://doi.org/10.1002/9780470015902.a0021231.pub2
  • Petta JC, Shipley ON, Wintner SP, Cliff G, Dicken ML, Hussey NE (2020) Are you really what you eat? Stomach content analysis and stable isotope ratios do not uniformly estimate dietary niche characteristics in three marine predators. Oecologia 192(4): 1111-1126. https://doi.org/10.1007/s00442-020-04628-6
    » https://doi.org/10.1007/s00442-020-04628-6
  • Phillips DL (2012) Converting isotope values to diet composition: the use of mixing models. Journal of Mammalogy 93(2): 342-352. https://doi.org/10.1644/11-MAMM-S-158.1
    » https://doi.org/10.1644/11-MAMM-S-158.1
  • Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261-269. https://doi.org/10.1007/s00442-003-1218-3
    » https://doi.org/10.1007/s00442-003-1218-3
  • Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92(10): 823-835. https://doi.org/10.1139/cjz-2014-0127
    » https://doi.org/10.1139/cjz-2014-0127
  • Post DM (2002) Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83(3): 703. https://doi.org/10.2307/3071875
    » https://doi.org/10.2307/3071875
  • Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Marine Biology 155: 593-598.
  • Revelle R, Suess HE (1957) Carbon dioxide exchange between atmosphere and ocean and the question of an increase of atmospheric CO2 during the past decades. Tellus 9(1): 18-27. https://doi.org/10.1111/j.2153-3490.1957.tb01849.x
    » https://doi.org/10.1111/j.2153-3490.1957.tb01849.x
  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142(6): 1141-1153. https://doi.org/10.1016/j.biocon.2009.02.021
    » https://doi.org/10.1016/j.biocon.2009.02.021
  • Rocque DA, Winker K (2005) Use of Bird Collections in Contaminant and Stable-Isotope Studies. Auk 122(3): 990-994.
  • Ross JD, Kelly JF, Bridge ES, Engel MH, Reinking DL, Boyle WA (2015) Pallid bands in feathers and associated stable isotope signatures reveal effects of severe weather stressors on fledgling sparrows. PeerJ 3: e814. https://doi.org/10.7717/peerj.814
    » https://doi.org/10.7717/peerj.814
  • Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology and Evolution 19(5): 256-63. https://doi.org/10.1016/j.tree.2004.03.017
    » https://doi.org/10.1016/j.tree.2004.03.017
  • Rutkowska M, Płotka-Wasylka J, Lubinska-Szczygeł M, Różańska A, Możejko-Ciesielska J, Namieśnik J (2018) Birds’ feathers - Suitable samples for determination of environmental pollutants. Trends in Analytical Chemistry 109: 97-115. https://doi.org/10.1016/j.trac.2018.09.022
    » https://doi.org/10.1016/j.trac.2018.09.022
  • Sales LP, Galetti M, Pires MM (2020) Climate and land-use change will lead to a faunal “savannization” on tropical rainforests. Global Change Biology 26(12): 7036-7044. https://doi.org/10.1111/gcb.15374
    » https://doi.org/10.1111/gcb.15374
  • Sena-Souza JP, Costa FJV, Nardoto GB (2019) Background and the use of isoscapes in the Brazilian context: essential tool for isotope data interpretation and natural resource management. Ambiente e Agua - An Interdisciplinary Journal of Applied Science 14(2): 1. https://doi.org/10.4136/ambi-agua.2282
    » https://doi.org/10.4136/ambi-agua.2282
  • Silvério DV, Brando PM, Balch JK, Putz FE, Nepstad DC, Oliveira-Santos C, Bustamante MMC (2013) Testing the Amazon savannization hypothesis: fire effects on invasion of a neotropical forest by native cerrado and exotic pasture grasses. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20120427. https://doi.org/10.1098/rstb.2012.0427
    » https://doi.org/10.1098/rstb.2012.0427
  • Siqueira PR, Vasconcelos MF, Gonçalves RMM, Leite LO (2015) Assessment of stomach contents of some amazonian birds. Ornitología Neotropical 26: 79-88.
  • Smith TB, Marra PP, Webster MS, Lovette I, Gibbs HL, Holmes RT, Hobson KA, Rohwer S (2003) A call for feather sampling. Auk 120(1): 218-221. https://doi.org/10.2307/4090162
    » https://doi.org/10.2307/4090162
  • Somenzari M, Amaral PP, Cueto VR, Guaraldo ADC, Jahn AE, Lima DM, Lima PC, Lugarini C, Machado CG, Martinez J, Nascimento JLX, Pacheco JF, Paludo D, Prestes NP, Serafini PP, Silveira LF, Sousa AEBA, Sousa NA, Souza MA, Telino-Júnior WR, Whitney BM (2018) An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia 58: 3. https://doi.org/10.11606/1807-0205/2018.58.03
    » https://doi.org/10.11606/1807-0205/2018.58.03
  • Sousa AEBA, Pereira PS (2020) Manual de anilhamento de aves silvestres. ICMBio-CEMAVE, Brasília, Brazil, 113 pp.
  • Stock BC, Jackson AL, Ward EJ, Parnell AC, Phillips DL, Semmens BX (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6: e5096. https://doi.org/10.7717/peerj.5096
    » https://doi.org/10.7717/peerj.5096
  • Symes CT (2012) Stable Isotope Research in Southern African Birds. In: Ali M (Ed.) Diversity of Ecosystems. IntechOpen, London, 251-288.
  • Tawa K, Sagawa S (2021) Stable isotopic analysis of stuffed specimens revealed the feeding habits of Oriental Storks Ciconia boyciana in Japan before their extinction in the wild. Journal of Ornithology 162: 193-206. https://doi.org/10.1007/s10336-020-01806-4
    » https://doi.org/10.1007/s10336-020-01806-4
  • Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS One 10(1): e0116182. https://doi.org/10.1371/journal.pone.0116182
    » https://doi.org/10.1371/journal.pone.0116182
  • Villegas M, Newsome SD, Blake JG (2016) Seasonal patterns in δ2H values of multiple tissues from Andean birds provide insights into elevational migration. Ecological Applications 26(8): 2383-2389.
  • Vitória AP, Ávila-Lovera E, Oliveira Vieira T, Couto-Santos APL, Pereira TJ, Funch LS, Freitas L, Miranda LDAP, Rodrigues PJFP, Rezende CE, Santiago LS (2018) Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) of deciduous and evergreen understorey trees in two tropical Brazilian Atlantic forests. Journal of Tropical Ecology 34(2): 145-156. https://doi.org/10.1017/S0266467418000093
    » https://doi.org/10.1017/S0266467418000093
  • Whiteman J, Elliott Smith E, Besser A, Newsome S (2019) A Guide to Using Compound-Specific Stable Isotope Analysis to Study the Fates of Molecules in Organisms and Ecosystems. Diversity 11(1): 8. https://doi.org/10.3390/d11010008
    » https://doi.org/10.3390/d11010008
  • Wiley AE, James HF, Ostrom PH (2017) Emerging techniques for isotope studies of avian ecology. In: Webster MS (Ed.) The Extended specimen: emerging frontiers in collections-based ornithological research. CRC Press, Boca Raton, 89-109.
  • Winker K (2005) Bird Collections: Development and use of a scientific resource. Auk 122(3): 966-971. https://doi.org/10.1093/auk/122.3.966
    » https://doi.org/10.1093/auk/122.3.966
  • Yohannes E, Palinauskas V, Valkiūnas G, Lee RW, Bolshakov CV, Bensch S (2011) Does avian malaria infection affect feather stable isotope signatures? Oecologia 167(4): 937-942. https://doi.org/10.1007/s00442-011-2041-x
    » https://doi.org/10.1007/s00442-011-2041-x

ADDITIONAL NOTES

  • Zoobank register

    http://zoobank.org/176323A1-9571-4986-B6D0-3C64E95EC308
  • How to cite this article

    Navarro AB, Magioli M, Moreira MZ, Silveira LF (2022) Perspectives and challenges on isotopic ecology of terrestrial birds in Brazil. Zoologia (Curitiba) 39: e21023. https://doi.org/10.1590/S1984-4689.v39.e21023
  • Published by

    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

Publication Dates

  • Publication in this collection
    16 May 2022
  • Date of issue
    2022

History

  • Received
    01 Sept 2021
  • Accepted
    31 Jan 2022
Sociedade Brasileira de Zoologia Caixa Postal 19020, 81531-980 Curitiba PR Brasil, Tel./Fax: (55 41) 3266-6823 - Curitiba - PR - Brazil
E-mail: sbz@sbzoologia.org.br