Abstract
Deforestation and habitat loss resulting from land use changes are some of the utmost anthropogenic impacts that threaten tropical birds in human-modified landscapes (HMLs). The degree of these impacts on birds’ diet, habitat use, and ecological niche can be measured by isotopic analysis. We investigated whether the isotopic niche width, food resources, and habitat use of bird trophic guilds differed between HMLs and natural landscapes (NLs) using stable carbon (δ13C) and nitrogen isotopes (δ15N). We analyzed feathers of 851 bird individuals from 28 landscapes in the Brazilian Atlantic Forest. We classified landscapes into two groups according to the percentage of forest cover (HMLs ≤ 30%; NLs ≥ 47%), and compared the isotopic niche width and mean values of δ13C and δ15N for each guild between landscape types. The niches of frugivores, insectivores, nectarivores, and omnivores were narrower in HMLs, whereas granivores showed the opposite pattern. In HMLs, nectarivores showed a reduction of 44% in niche width, while granivores presented an expansion of 26%. Individuals in HMLs consumed more resources from agricultural areas (C4 plants), but almost all guilds showed a preference for forest resources (C3 plants) in both landscape types, except granivores. Degraded and fragmented landscapes typically present a lower availability of habitat and food resources for many species, which was reflected by the reduction in niche width of birds in HMLs. Therefore, to protect the diversity of guilds in HMLs, landscape management strategies that offer birds more diverse habitats must be implemented in tropical regions.
Similar content being viewed by others
Data availability
All data produced from this study are provided in this manuscript and its supplementary material.
Code availability
Not applicable.
References
Aguiar AP, Chiarello AG, Mendes SL, Matos ED (2003) The central and Serra do Mar corridors in the Brazilian Atlantic forest. In: Galindo-Leal C, Câmara IG (eds) The Atlantic forest of South America: biodiversity status, threats and outlook center for applied biodiversity science at conservation international. Island Press, Washington, EUA, pp 118–132
Alexandrino ER, Buechley ER, Karr JR et al (2017) Bird based index of biotic integrity : assessing the ecological condition of Atlantic forest patches in human-modified landscape. Ecol Indic 73:662–675. https://doi.org/10.1016/j.ecolind.2016.10.023
Araújo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958. https://doi.org/10.1111/j.1461-0248.2011.01662.x
Augusto FG, Filho MT, Ferreira A et al (2015) Land use change in the Atlantic forest affects carbon and nitrogen sources of streams as revealed by the isotopic composition of terrestrial invertebrates. Biota Neotrop 15:e20140188. https://doi.org/10.1590/1676-06032015018814
Barros FM, Peres CA, Pizo MA, Ribeiro MC (2019) Divergent flows of avian-mediated ecosystem services across forest-matrix interfaces in human-modified landscapes. Landsc Ecol 34:879–894. https://doi.org/10.1007/s10980-019-00812-z
Barton K (2020) Package ‘MuMIn’: multi-model inference. R package version 1.43.17. https://cran.r-project.org/package=MuMIn. Accessed 10 Nov 2020
Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst 42:411–440
Boesing AL, Marques TS, Martinelli LA et al (2021) Conservation implications of a limited avian cross-habitat spillover in pasture lands. Biol Conserv 253:108898
Bogoni JA, da Silva PG, Peres CA (2019) Co-declining mammal–dung beetle faunas throughout the Atlantic forest biome of South America. Ecography 42:1803–1818. https://doi.org/10.1111/ecog.04670
Bregman TP, Sekercioglu CH, Tobias JA (2014) Global patterns and predictors of bird species responses to forest fragmentation: implications for ecosystem function and conservation. Biol Conserv 169:372–383. https://doi.org/10.1016/j.biocon.2013.11.024
Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach, second. Springer, Fort Collins
Carrara E, Arroyo-Rodríguez V, Vega-Rivera JH et al (2015) Impact of landscape composition and configuration on forest specialist and generalist bird species in the fragmented Lacandona rainforest, Mexico. Biol Conserv 184:117–126. https://doi.org/10.1016/j.biocon.2015.01.014
Carvalho DR, Castro D, Callisto M et al (2015) Isotopic variation in five species of stream fishes under the influence of different land uses. J Fish Biol 87:559–578. https://doi.org/10.1111/jfb.12734
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. J Appl Ecol 46:443–453. https://doi.org/10.1111/j.1365-2664.2009.01620.x
Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. The University of Chicago Press, Chicago, IL
da Silva BG, Koch I, Piratelli AJ (2020) Fruit and flower availability affect bird assemblages across two successional stages in the Atlantic forest. Stud Neotrop Fauna Environ 00:1–13. https://doi.org/10.1080/01650521.2020.1743550
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117:507–514. https://doi.org/10.1111/j.2008.0030-1299.16215.x
Estavillo C, Pardini R, da Rocha PLB (2013) Forest loss and the biodiversity threshold: an evaluation considering species habitat requirements and the use of matrix habitats. PLoS ONE 8:e82369. https://doi.org/10.1371/journal.pone.0082369
Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet earth. Science 333:301–306. https://doi.org/10.1126/science.1205106
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/132419
Farina A (2006) Principles and methods in landscape ecology. Springer, Dordrecht, The Netherlands
FBDS (2019) The Brazilian foundation for sustainable development. https://www.fbds.org.br/article.php3?id_article=594. Accessed 13 Aug 2019
Ferger SW, Bohning-Gaese K, Wilcke W et al (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
Galetti M, Rodarte RR, Neves CL et al (2016) Trophic niche differentiation in rodents and marsupials revealed by stable isotopes. PLoS ONE 11:1–15. https://doi.org/10.1371/journal.pone.0152494
Giraudo AR, Matteucci SD, Alonso J et al (2008) Comparing bird assemblages in large and small fragments of the Atlantic forest hotspots. Biodivers Conserv 17:1251–1265. https://doi.org/10.1007/s10531-007-9309-9
González-Carcacía JA, Herrera MLG, Nassar JM (2020) Dietary importance of C3 and CAM food pathways for birds in a neotropical semiarid zone. Biotropica 00:1–8. https://doi.org/10.1111/btp.12798
Haddad NM, Brudvig LA, Clobert J et al (2015) Habitat fragmentation and its lasting impact on earth’s ecosystems. Sci Adv 1:e1500052. https://doi.org/10.1126/sciadv.1500052
Healy K, Guillerme T, Kelly SBAA et al (2017) SIDER: an R package for predicting trophic discrimination factors of consumers based on their ecology and phylogenetic relatedness. Ecography 41:1–7. 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. Environ Sci Technol 35:3482–3487. https://doi.org/10.1021/es001970p
Hendershot JN, Smith JR, Anderson CB et al (2020) Intensive farming drives long-term shifts in avian community composition. Nature 579:393–396. https://doi.org/10.1038/s41586-020-2090-6
Hobson KA (2011) Isotopic ornithology: a perspective. J Ornithol 152:S49–S66. https://doi.org/10.1007/s10336-011-0653-x
Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197
Hopkins JB, Ferguson JM (2012) Estimating the diets of animals using stable isotopes and a comprehensive Bayesian mixing model. PLoS ONE. 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
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Jesus FM, Pereira MR, Rosa CS et al (2015) Preservation methods alter carbon and nitrogen stable isotope values in crickets (Orthoptera: Grylloidea). PLoS ONE 10:e0137650. https://doi.org/10.1371/journal.pone.0137650
Lares B (2020) Package ‘lares’: analytics, data mining and machine learning sidekick. R package version 4.9.8. https://github.com/laresbernardo/lares. Accessed 18 Nov 2020
Long ES, Sweitzer RA, Diefenbach DR, Ben-David M (2005) Controlling for anthropogenically induced atmospheric variation in stable carbon isotope studies. Oecologia 146:148–156. https://doi.org/10.1007/s00442-005-0181-6
Lopes IT, Gussoni COA, Demarchi LO et al (2015) Diversity of understory birds in old stands of native and Eucalyptus plantations. Restor Ecol 23:662–669. https://doi.org/10.1111/rec.12216
Magioli M, Moreira MZ, Fonseca RCB et al (2019) Human-modified landscapes alter mammal resource and habitat use and trophic structure. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1904384116
Martensen AC, Ribeiro MC, Banks-Leite C et al (2012) Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conserv Biol 26:1100–1111. https://doi.org/10.1111/j.1523-1739.2012.01940.x
Martinelli LA, Ometto JPHB, Ferraz ES et al (2009) Desvendando questões ambientais com isótopos estáveis. Oficina de textos, São Paulo, Brazil
Martinelli LA, Nardoto GB, Soltangheisi A et al (2020) Determining ecosystem functioning in Brazilian biomes through foliar carbon and nitrogen concentrations and stable isotope ratios. Biogeochemistry 117:26842–26848. https://doi.org/10.1007/s10533-020-00714-2
Mittermeier RA, Turner WR, Larsen FW et al (2011) Global biodiversity conservation: the critical role of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer Publishers, London, UK, pp 3–22
Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480. https://doi.org/10.1111/j.1461-0248.2008.01163.x
Morante-Filho JC, Faria D, Mariano-Neto E, Rhodes J (2015) Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic forest. PLoS ONE 10:1–18. https://doi.org/10.1371/journal.pone.0128923
Morante-Filho JC, Arroyo-Rodríguez V, de SouzaPessoa M et al (2018) Direct and cascading effects of landscape structure on tropical forest and non-forest frugivorous birds. Ecol Appl 28:2024–2032. https://doi.org/10.1002/eap.1791
Motta Junior JC (1990) Estrutura trófica e composição das avifaunas de três habitats terrestres na região central do estado de São Paulo. Ararajuba 1:65–71
Newbold T, Scharlemann JPW, Butchart SHM et al (2013) Ecological traits affect the response of tropical forest bird species to land-use intensity. Proc R Soc B 280:1–8. https://doi.org/10.1098/rspb.2012.2131
Newbold T, Hudson LN, Hill SLL et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50. https://doi.org/10.1038/nature14324
Newsome SD, del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436. https://doi.org/10.1890/060150.01
Pagani-Núñez E, Liang D, He C et al (2019) Niches in the Anthropocene: passerine assemblages show niche expansion from natural to urban habitats. Ecography (Cop) 42:1–10. https://doi.org/10.1111/ecog.04203
Pardini R, Faria D, Accacio GM et al (2009) The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia. Biol Conserv 142:1178–1190. https://doi.org/10.1016/j.biocon.2009.02.010
Pecquerie L, Nisbet RM, Fablet R et al (2010) The impact of metabolism on stable isotope dynamics: a theoretical framework. Philos Trans R Soc B Biol Sci 365:3455–3468. https://doi.org/10.1098/rstb.2010.0097
Pfeifer M, Lefebvre V, Peres CA et al (2017) Creation of forest edges has a global impact on forest vertebrates. Nature 551:187–191. https://doi.org/10.1038/nature24457
Phillips DL, Inger R, Bearhop S et al (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 92:823–835. https://doi.org/10.1139/cjz-2014-0127
Piratelli AJ, Franchin AG, Marín-Gómez OH (2017) Urban conservation: toward bird-friendly cities in Latin America. In: MacGregor-Fors I, Escobar-Ibáñez JF (eds) Avian ecology in Latin American cityscapes. Springer International Publishing, Cham, Germany, pp 143–158
Pizo MA (2007) Frugivory by birds in degraded areas of Brazil. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI, Wallingford, UK, pp 615–627
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703. https://doi.org/10.2307/3071875
Powell RL, Yoo E-H, Still CJ (2012) Vegetation and soil carbon-13 isoscapes for South America: integrating remote sensing and ecosystem isotope measurements. Ecosphere 3:109. https://doi.org/10.1890/ES12-00162.1
QGIS (2018) Geographic information system. Open source geospatial foundation project. http://qgis.osgeo.org. Accessed 15 Dec 2018
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
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 9:18–27. https://doi.org/10.1111/j.2153-3490.1957.tb01849.x
Rezende CL, Scarano FR, Assad ED et al (2018) From hotspot to hopespot: an opportunity for the Brazilian Atlantic forest. Perspect Ecol Conserv 16:208–214. https://doi.org/10.1016/j.pecon.2018.10.002
Rigueira DMG, da Rocha PLB, Mariano-Neto E (2013) Forest cover, extinction thresholds and time lags in woody plants (Myrtaceae) in the Brazilian Atlantic forest: resources for conservation. Biodivers Conserv 22:3141–3163. https://doi.org/10.1007/s10531-013-0575-4
Ríos A, Manuel J (2012) Effects of nutritional and anti-nutritional properties of seeds on the feeding ecology of seed-eating birds of the Monte desert, Argentina. Condor 114:44–55. https://doi.org/10.1525/cond.2012.110043
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263. https://doi.org/10.1016/j.tree.2004.03.017
Sales LP, Galetti M, Pires MM (2020) Climate and land-use change will lead to a faunal “savannization” on tropical rainforests. Glob Chang Biol 26:7036–7044. https://doi.org/10.1111/gcb.15374
Scarano FR, Ceotto P (2015) Brazilian Atlantic forest: impact, vulnerability, and adaptation to climate change. Biodivers Conserv 24:2319–2331. https://doi.org/10.1007/s10531-015-0972-y
Scheele BC, Foster CN, Banks SC, Lindenmayer DB (2017) Niche contractions in declining species: mechanisms and consequences. Trends Ecol Evol 32:346–355. https://doi.org/10.1016/j.tree.2017.02.013
Sekercioglu CH (2006) Increasing awareness of avian ecological function. Trends Ecol Evol 21:464–471. https://doi.org/10.1016/j.tree.2006.05.007
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. Ambient Agua Interdiscip J Appl Sci 14:1. https://doi.org/10.4136/ambi-agua.2282
Sexton JP, Montiel J, Shay JE et al (2017) Evolution of ecological niche breadth. Annu Rev Ecol Evol Syst 48:183–206. https://doi.org/10.1146/annurev-ecolsys-110316-023003
Silvério DV, Brando PM, Balch JK et al (2013) Testing the Amazon savannization hypothesis: fire effects on invasion of a neotropical forest by native cerrado and exotic pasture grasses. Philos Trans R Soc B Biol Sci 368:20120427. https://doi.org/10.1098/rstb.2012.0427
Sirami C, Gross N, Baillod AB et al (2019) Increasing crop heterogeneity enhances multitrophic diversity across agricultural regions. Proc Natl Acad Sci 116:16442–16447. https://doi.org/10.1073/pnas.1906419116
Souza CM, Shimbo JZ, Rosa MR et al (2020) Reconstructing three decades of land use and land cover changes in Brazilian biomes with landsat archive and earth engine. Remote Sens 12:2735. https://doi.org/10.3390/rs12172735
Steffen W, Sanderson A, Tyson PD et al (2005) Global change and the earth system: a planet under pressure, 2nd edn. Springer, Berlin, Germany
Stock BC, Jackson AL, Ward EJ et al (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6:e5096. https://doi.org/10.7717/peerj.5096
Strasser H, Weber C (1999) On the asymptotic theory of permutation statistics. Math Methods Stat 8:220–250
Uezu A, Metzger JP (2011) Vanishing bird species in the Atlantic forest: relative importance of landscape configuration, forest structure and species characteristics. Biodivers Conserv 20:3627–3643. https://doi.org/10.1007/s10531-011-0154-5
Vellend M, Baeten L, Becker-Scarpitta A et al (2017) Plant biodiversity change across scales during the Anthropocene. Annu Rev Plant Biol 68:563–586. https://doi.org/10.1146/annurev-arplant-042916-040949
Victor MAM, Cavalli AC, Guillaumon JR, Serra Filho R (2005) Cem anos de devastação: revisitada 30 anos depois. Ministério do Meio Ambiente, Brasília, Brazil
Vitória AP, Ávila-Lovera E, De Oliveira VT et al (2018) Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) of deciduous and evergreen understorey trees in two tropical Brazilian Atlantic forests. J Trop Ecol 34:145–156. https://doi.org/10.1017/S0266467418000093
Wiley AE, Ostrom PH, Stricker CA et al (2010) Isotopic characterization of flight feathers in two pelagic seabirds: sampling strategies for ecological studies. Condor 112:337–346. https://doi.org/10.1525/cond.2010.090186
Willis EO (1979) The composition of avian communities in remanescent woodlots in southern Brasil. Pap Avulsos Zool 33:1–25
Wilman H, Belmaker J, Simpson J et al (2014) EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027–2027. https://doi.org/10.1890/13-1917.1
Acknowledgements
We sincerely thank the people that helped this research, without knowing they were doing it, through depositing specimens of birds in MZUSP collections (Museum of Zoology of the University of São Paulo, Brazil). All the authors thank São Paulo Research Foundation (FAPESP), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico (CNPq) for the financial support. We thank the reviewers who provided helpful feedback to improve our manuscript.
Funding
São Paulo Research Foundation (FAPESP) provided financial support that allowed the data collection (#2010/05343-5, #2011/06782-5 and #2011/04046-0). ABN was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code #88882.328664/2019-01). ABN is supported by a doctoral scholarship from FAPESP (process #2020/07619-0). JAB is supported by a postdoctoral fellowship grant from FAPESP (#2018-05970-1). ERA is founded by Conselho Nacional de Pesquisa e Desenvolvimento Científico e Tecnológico (CNPq) research grant (#300744/2020-0—Programa de Capacitação Institucional). ERA also was supported by CAPES during his postdoctoral research (Finance Code 001—CAPES PNPD 2013/1723). CNPq provided research grants for KMPMBF (#308632/2018-4), LFS (#302291/2015-6 and #308337/2019-0) and MAP (#304742/2019-8).
Author information
Authors and Affiliations
Contributions
ABN, KMPMBF, MZM, LFS, MAP and WRS conceived the ideas and designed methodology; ABN, LFS, ERA, DTAL, MAP, VCO, RJD, AVC and AJP collected the data; ABN, MM and JAB analyzed the data; ABN led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Ethical approval
Ethics approval for this study was waived by ICMBio according to IN 3/2014 and RN 18/2014.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Seth Newsome.
In memoriam Daniela Tomasio Apolinario da Luz.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Navarro, A.B., Magioli, M., Bogoni, J.A. et al. Human-modified landscapes narrow the isotopic niche of neotropical birds. Oecologia 196, 171–184 (2021). https://doi.org/10.1007/s00442-021-04908-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-021-04908-9