Biodiversity and Conservation

, Volume 28, Issue 12, pp 3371–3386 | Cite as

Interspecific networks of cavity-nesting vertebrates reveal a critical role of broadleaf trees in endangered Araucaria mixed forests of South America

  • Kristina L. CockleEmail author
  • José Tomás Ibarra
  • Tomás A. Altamirano
  • Kathy Martin
Original Paper
Part of the following topical collections:
  1. Forest and plantation biodiversity


Cavity-nesting animals and their nest trees are linked in interspecific facilitation networks known as nest webs, which play key roles in forest function but vary across biomes and with human perturbation. We examined the composition, structure and function of nest webs between two endangered old-growth forests representing the last remnants of the ancient coniferous family Araucariaceae in South America: pewen (Araucaria araucana; Endangered) in temperate Chile (2010–2018), and Parana pine (Araucaria angustifolia; Critically Endangered) in subtropical Argentina (2006–2018). Pewen and Parana pine accounted for 30 and 9% of forest basal area, but only 2 and 5% of nesting cavities, respectively. Instead, cavity-nesting birds and mammals nested disproportionately in coexisting broadleaf trees. Species richness, interaction richness, and mean number of links per species were much higher in Parana pine forest than in pewen forest, but the two nest webs had similar levels of evenness and nestedness. Most secondary cavity-nesting species depended on cavities formed by decay in Nothofagus spp. (98% of nest cavities in pewen forest) or Apuleia leiocarpa (26% of nest cavities in Parana pine forest). An exception was the globally endangered Vinaceous Parrot, a Parana pine seed disperser, which made 50% of its nests in decay-formed cavities in Parana pine. To conserve the ecosystem functions of endangered Araucaria forests it is important to protect and recruit not only Araucaria trees but also a mix of broadleaf trees that can confer resilience to nest webs in the face of major disturbances.


Cavity-nesting birds Ecological network Interspecific interactions Neotropics Nest web Old-growth forest 



We are grateful to all colleagues and assistants who helped with field work and shared data over the many years of our study, including, in recent years, Alejandro Bodrati, Bianca Bonaparte, Facundo Di Sallo, Carlos Ferreyra, Milka Gómez, Helene Jaillard, Martjan Lammertink, Fernando Novoa, Constanza Rivas, and Alejandra Vermehren. This study was funded by Columbus Zoo and Aquarium, Rufford Small Grants for Nature Conservation (14397-2 and 18013-D), “NETBIOAMERICAS” CONICYT/Apoyo a la Formación de Redes Internacionales entre Centros de Investigación (REDES150047), PICT (2016-0144), Riverbanks Conservation Support Fund, Fresno Chaffee Zoo Wildlife Conservation Fund, Minnesota Zoo Foundation, and CONICYT/FONDECYT de Inicio (11160932). TAA was supported by a Postdoctoral scholarship from CONICYT (74160073).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Field work was authorized by Ministerio de Ecología y RNR (Misiones, Argentina) and Corporación Nacional Forestal (CONAF; Permits 11/2012, 13/2015, 02/2016 IX; Chile) and complied with the current laws of Argentina and Chile. All applicable international, national, and institutional guidelines for the care and use of animals were followed.

Supplementary material

10531_2019_1826_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)


  1. Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335:1486–1489CrossRefPubMedGoogle Scholar
  2. Alarcón D, Cavieres LA (2015) In the right place at the right time: habitat representation in protected areas of South American Nothofagus-dominated plants after a dispersal constrained climate change scenario. PLoS ONE 10:e0119952CrossRefPubMedPubMedCentralGoogle Scholar
  3. Altamirano TA, Ibarra JT, Martin K, Bonacic C (2017) The conservation value of tree decay processes as a key driver structuring tree cavity nest webs in South American temperate rainforests. Biodivers Conserv 26:2453–2472CrossRefGoogle Scholar
  4. Armesto JJ, Smith-Ramírez C, Carmona MR, Celis-Diez JL, Díaz IA, Gaxiola A, Gutiérrez AG, Núñez-Avila MC, Pérez CA, Rozzi R (2009) Old-growth temperate rainforests of South America: conservation, plant-animal interactions, and baseline biogeochemical processes. In: Wirth C, Gleixner G, Heimann M (eds) Old-growth forests function, fate and value. Springer, Berlin, pp 367–390CrossRefGoogle Scholar
  5. Bai M-L, Wichmann F, Mühlenberg (2005) Nest-site characteristics of hole-nesting birds in a primeval boreal forest of Mongolia. Acta Ornithol 40:1–14CrossRefGoogle Scholar
  6. Blanc LA, Walters JR (2007) Cavity-nesting community webs as predictive tools: where do we go from here? J Ornithol 148(Suppl 2):S417–S423CrossRefGoogle Scholar
  7. Blanc LA, Walters JR (2008a) Cavity excavation and enlargement as mechanisms for indirect interactions in an avian community. Ecology 89:506–514CrossRefGoogle Scholar
  8. Blanc LA, Walters JR (2008b) Cavity-nest webs in a longleaf pine ecosystem. Condor 110:80–92CrossRefGoogle Scholar
  9. Bodrati A, Cockle K, Segovia JM, Roesler I, Areta JI, Jordan E (2010) The avifauna of Parque Provincial Cruce Caballero, Province of Misiones, Argentina. Cotinga 32:41–64Google Scholar
  10. Carneiro APB, Jiménez JE, Vergara PM, White TH Jr (2013) Nest-site selection by Slender-billed Parakeets in a Chilean agricultural-forest mosaic. J Field Ornithol 84:13–22CrossRefGoogle Scholar
  11. Cockle KL, Martin K (2015) Temporal dynamics of a commensal network of cavity-nesting vertebrates: increased diversity during an insect outbreak. Ecology 96:1093–1104CrossRefGoogle Scholar
  12. Cockle K, Capuzzi G, Bodrati A, Clay R, del Castillo H, Velázquez M, Areta JI, Fariña N, Fariña R (2007) Distribution, abundance, and conservation of Vinaceous Amazons in Argentina and Paraguay. J Field Ornithol 78:21–39CrossRefGoogle Scholar
  13. Cockle KL, Martin K, Drever MC (2010) Supply of tree-holes limits nest density of cavity-nesting birds in primary and logged subtropical Atlantic forest. Biol Conserv 143:2851–2857CrossRefGoogle Scholar
  14. Cockle K, Martin K, Wiebe K (2011a) Selection of nest trees by cavity-nesting birds in the Neotropical Atlantic forest. Biotropica 43:228–236CrossRefGoogle Scholar
  15. Cockle KL, Martin K, Wesołowski T (2011b) Woodpeckers, decay, and the future of cavity-nesting vertebrate communities worldwide. Front Ecol Environ 9:377–382CrossRefGoogle Scholar
  16. Cockle KL, Martin K, Robledo G (2012) Linking fungi, trees, and hole-using birds in a Neotropical tree-cavity network: pathways of cavity production and implications for conservation. For Ecol Manag 264:210–219CrossRefGoogle Scholar
  17. Collar NJ, Gonzaga LP, Krabbe N, Madroño Nieto A, Naranjo LG, Parker TA III, Wege DC (1992) Threatened birds of the Americas, the ICBP/IUCN RedData Book 2, 3rd edn. International Council for Bird Preservation, CambridgeGoogle Scholar
  18. DeGraaf RM, Shigo AL (1985) Managing cavity trees for wildlife in the Northeast. US Forest Service Gen Tech Rep NE-101Google Scholar
  19. Dénes FV, Tella JL, Zulian V, Prestes NP, Martínez J, Hiraldo F (2018) Combined impacts of multiple non-native mammals on two life stages of a critically endangered Neotropical tree. Biol Invasions 20:3055–3068CrossRefGoogle Scholar
  20. Díaz S, Kitzberger T (2013) Nest habitat selection by the austral parakeet in north-western Patagonia. Austral Ecol 38:268–278CrossRefGoogle Scholar
  21. Donoso C (1993) Bosques templados de Chile y Argentina: variación, estrutura y dinámica. Editorial Universitaria, SantiagoGoogle Scholar
  22. Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite package: analysing ecological networks. R News 8(2):8–11Google Scholar
  23. Drever MC, Aitken KEH, Norris AR, Martin K (2008) Woodpeckers as reliable indicators of bird richness, forest health and harvest. Biol Conserv 141:624–634CrossRefGoogle Scholar
  24. Emer C, Galetti M, Pizo MA, Jordano P, Verdú M (2019) Defaunation precipitates the extinction of evolutionarily distinct interactions in the Anthropocene. Sci Adv 5:eaav6699CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fang Y-T, Tuanmu M-N, Hung C-M (2018) Asynchronous evolution of interdependent nest characters across the avian phylogeny. Nat Commun 9:1863CrossRefPubMedPubMedCentralGoogle Scholar
  26. Galeano J, Pastor JM, Iriondo JM (2008) Weighted-Interaction Nestedness Estimator (WINE): a new estimator to calculate over frequency matrices. arXiv 0808.3397v2 []Google Scholar
  27. Gibbons P, Lindenmayer D (2002) Tree hollows and wildlife conservation in Australia. CSIRO, CollingwoodCrossRefGoogle Scholar
  28. González ME, Veblen TT, Sibold JS (2010) Influence of fire severity on stand development of Araucaria araucana-Nothofagus pumilio stands in the Andean cordillera of south-central Chile. Austral Ecol 35:597–615CrossRefGoogle Scholar
  29. Herrmann TM (2006) Indigenous knowledge and management of Araucaria araucana forest in the Chilean Andes: implications for native forest conservation. Biodivers Conserv 15:647–662CrossRefGoogle Scholar
  30. Hueck K (1972) As florestas da América do Sul. Editora da Universidade de Brasília/Editora Polígono, São PauloGoogle Scholar
  31. Ibarra JT, Martin K (2015) Biotic homogenization: loss of avian functional richness and habitat specialists in disturbed Andean temperate forests. Biol Conserv 192:418–427CrossRefGoogle Scholar
  32. Ibarra JT, Altamirano T, Gálvez N, Rojas I, Laker J, Bonacic C (2010) Avifauna de los bosques templados de Araucaria araucana del sur de Chile. Ecol Austral 20:33–45Google Scholar
  33. Ibarra JT, Martin M, Cockle KL, Martin K (2017) Maintaining ecosystem resilience: functional responses of tree cavity nesters to logging in temperate forests of the Americas. Sci Rep 7:4467CrossRefPubMedPubMedCentralGoogle Scholar
  34. Ilsøe SK, Kissling WD, Fjeldså JF, Sandel B, Svenning J-C (2017) Global variation in woodpecker species richness shaped by tree availability. J Biogeogr 44:1824–1835CrossRefGoogle Scholar
  35. IUCN (2018) The IUCN red list of threatened species. Version 2018-2. Accessed 2 Dec 2018
  36. Jiménez JE, White TH Jr (2011) Use of tree cavities for nesting by Speckled Teal (Anas flavirostris) in southern Chile: potential competition with Slender-billed Parakeets (Enicognathus leptorhynchus). Ornitol Neotrop 22:465–469Google Scholar
  37. Kershaw P, Wagstaff B (2001) The southern conifer family Araucariaceae: history, status, and value for paleoenvironmental reconstruction. Annu Rev Ecol Syst 32:397–414CrossRefGoogle Scholar
  38. Koch AJ, Munks SA, Driscoll D, Kirkpatrick JB (2008) Does hollow occurrence vary with forest type? A case study in wet and dry Eucalyptus obliqua forest. For Ecol Manag 255:3938–3951CrossRefGoogle Scholar
  39. Lacerda AEB (2016) Conservation strategies for Araucaria forests in southern Brazil: assessing current and alternative approaches. Biotropica 48:537–544CrossRefGoogle Scholar
  40. Lammertink M, Prawiradilaga DM, Setiorini U, Naing TZ, Duckworth JW, Menken SBJ (2009) Global population decline of the Great Slaty Woodpecker (Mulleripicus pulverulentus). Biol Conserv 142:166–179CrossRefGoogle Scholar
  41. Looy CV (2013) Natural history of a plant trait: branch-system abscission in Paleozoic conifers and its environmental, autecological, and ecosystem implications in a fire-prone world. Paleobiology 39:235–252CrossRefGoogle Scholar
  42. Martin TE (2014) Consequences of habitat change and resource selection specialization for population limitation in cavity-nesting birds. J Appl Ecol 252:475–485Google Scholar
  43. Martin K, Eadie JM (1999) Nest webs: a community-wide approach to the management and conservation of cavity-nesting forest birds. For Ecol Manag 115:243–257CrossRefGoogle Scholar
  44. Martin K, Aitken KEH, Wiebe KL (2004) Nest sites and nest webs for cavity-nesting communities in interior British Columbia, Canada: nest characteristics and niche partitioning. Condor 106:5–19CrossRefGoogle Scholar
  45. Martín González AA, Dalsgaard B, Nogués-Bravo D et al (2015) The macroecology of phylogenetically structured hummingbird–plant networks. Glob Ecol Biogeogr 24:1212–1224CrossRefGoogle Scholar
  46. Maruyama PK, Vizentin-Bugoni J, Sonne J et al (2016) The integration of alien plants in mutualistic plant-hummingbird networks across the Americas: the importance of species traits and insularity. Divers Distrib 22:672–681CrossRefGoogle Scholar
  47. Medina-Macedo L, Biscaia de Lacerda AE, Sebbenn AM, Zanetti Ribeiro J, Soccol CR, Messias Bittencourt JV (2016) Using genetic diversity and mating system parameters estimated from genetic markers to determine strategies for the conservation of Araucaria angustifolia (Bert.) O. Kuntze (Araucariaceae). Conserv Genet 17:413–423CrossRefGoogle Scholar
  48. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717CrossRefPubMedGoogle Scholar
  49. Millington WF, Chaney WR (1973) Shedding of shoots and branches. In: Kozlowski TT (ed) Shedding of plant parts. Physiological ecology. Academic Press, New YorkGoogle Scholar
  50. Monterrubio-Rico TC, Escalante-Pliego P (2006) Richness, distribution and conservation status of cavity-nesting birds in Mexico. Biol Conserv 128:67–78CrossRefGoogle Scholar
  51. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  52. Norris AR, Martin K (2012) Red-breasted nuthatches (Sitta canadensis) increase cavity excavation in response to a mountain pine beetle (Dendroctonus ponderosae) outbreak. Ecoscience 19:308–315CrossRefGoogle Scholar
  53. Panti C, Pujana RR, Zamaloa MC, Romero EJ (2012) Araucariaceae macrofossil record from South America and Antarctica. Alcheringa 36:1–22CrossRefGoogle Scholar
  54. Pauchard A, Villarroel P (2002) Protected areas in Chile: history, current status, and challenges. Nat Areas J 22:318–330Google Scholar
  55. Politi N, Hunter M Jr, Rivera L (2012) Assessing the effects of selective logging on birds in Neotropical piedmont and cloud montane forests. Biodivers Conserv 21:3131–3155CrossRefGoogle Scholar
  56. Prestes NP, Martinez J, Kilpp JC, Batistela T, Turkievicz A, Rezende E, Gaboardi VTR (2014) Ecologia e conservação de Amazona vinacea em áreas simpátricas com Amazona pretrei. Ornithologia 6:109–120Google Scholar
  57. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  58. Ragonese AE, Castiglioni JA (1946) Los pinares de Araucaria angustifolia en la República Argentina. Bol Soc Argent Bot 1:126–147Google Scholar
  59. Regos A, Imbeau L, Desrochers M, Leduc A, Robert M, Jobin B, Brotons L, Drapeau P (2018) Hindcasting the impacts of land-use changes on bird communities with species distribution models of Bird Atlas data. Ecol Appl 28:1867–1883CrossRefPubMedGoogle Scholar
  60. Ribeiro MC, Metzger JP, Camargo Martensen A, Ponzini FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  61. Ríos RC, Galvão F, Ribas Curcio G (2010) Estructura de las principales especies arbóreas en el Parque Provincial Cruce Caballero y su similitud florística con áreas de Argentina y de Brasil. Ciência Florestal, Santa Maria 20:193–206Google Scholar
  62. Robinson M, De Souza JG, Maezumi SY, Cardenas M, Pessenda L, Prufer K, Corteletti R, Scunderlick D, Mayle FE, De Blasis P, Iriarte J (2018) Uncoupling human and climate drivers of late Holocene vegetation change in southern Brazil. Sci Rep 8:7800CrossRefPubMedPubMedCentralGoogle Scholar
  63. Rodríguez-Cabal M, Nuñez M, Martínez AS (2008) Quantity versus quality: endemism and protected areas in the temperate forest of South America. Austral Ecol 33:730–736CrossRefGoogle Scholar
  64. Rother DC, Pizo MA, Jordano P (2016) Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages. Oikos 125:336–342CrossRefGoogle Scholar
  65. Ruggera RA, Schaaf AA, Vivanco CG, Politi N, Rivera LO (2016) Exploring nest webs in more detail to improve forest management. For Ecol Manag 372:93–100CrossRefGoogle Scholar
  66. Schunck F, Somenzari M, Lugarini C, Soares ES (2011) Plano de açao nacional para a conservação dos papagaios da Mata Atlântica. Centro Nacional de Pesquisa e Conservação de Aves Silvestres, BrasíliaGoogle Scholar
  67. Sedrez dos Reis M, Ladio A, Peroni N (2014) Landscapes with Araucaria in South America: evidence for a cultural dimension. Ecol Soc 19:43CrossRefGoogle Scholar
  68. Sick H (1993) Birds in Brazil: a natural history. Princeton University Press, PrincetonGoogle Scholar
  69. Soto GE, Vergara PM, Rodewald AD (2018) The fruit of competition: seed dispersal by Magellanic Woodpeckers in the threatened Valdivian Rainforest. Ecology 99:2617–2620CrossRefPubMedGoogle Scholar
  70. Speziale KL, Lambertucci SA, Gleiser G, Tella JL, Hiraldo F, Aizen MA (2018) An overlooked plant–parakeet mutualism counteracts human overharvesting on an endangered tree. R Soc Open Sci 5:171456CrossRefPubMedPubMedCentralGoogle Scholar
  71. Stotz DF, Fitzpatrick JW, Parker TA III, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press, ChicagoGoogle Scholar
  72. Tella JL, Dénes FV, Zulian V, Prestes NP, Martinez J, Blanco G, Hiraldo F (2016a) Endangered plant-parrot mutualisms: seed tolerance to predation makes parrots pervasive dispersers of the Parana pine. Sci Rep 6:31709CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tella JL, Lambertucci SA, Speziale KL, Hiraldo F (2016b) Large-scale impacts of multiple co-occurring invaders on monkey puzzle forest regeneration, native seed predators and their ecological interactions. Glob Ecol Conserv 6:1–15CrossRefGoogle Scholar
  74. Trøjelsgaard K, Jordano P, Carstensen DW, Olesen JM (2015) Geographical variation in mutualistic networks: similarity, turnover and partner fidelity. Proc R Soc B 282:20142925CrossRefPubMedGoogle Scholar
  75. Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279CrossRefGoogle Scholar
  76. van der Hoek Y, Gaona GV, Martin K (2017) The diversity, distribution and conservation status of the tree-cavity-nesting birds of the world. Divers Distrib 23:1120–1131CrossRefGoogle Scholar
  77. Veblen TT (1982) Regeneration patterns in Araucaria araucana forests in Chile. J Biogeogr 9:11–28CrossRefGoogle Scholar
  78. Wesołowski T, Martin K (2018) Tree holes and hole-nesting birds in European and North American forests. In: Mikusiński G, Roberge J-M, Fuller RJ (eds) Ecology and conservation of forest birds. Cambridge University Press, CambridgeGoogle Scholar
  79. White TH Jr, Jiménez JE (2017) Lophozonia tree cavities used for nesting by Slender-billed Parakeets (Enicognathus leptorhynchus) in the central valley of southern Chile: a potentially vanishing keystone resource. Avian Res 8:3CrossRefGoogle Scholar
  80. Wiebe KL (2016) Northern flickers only work when they have to: how individual traits, population size and landscape disturbances affect excavation rates of an ecosystem engineer. J Avian Biol 48:431–438CrossRefGoogle Scholar
  81. Zamorano-Elgueta C, Cayuela L, González-Espinosa M et al (2012) Impacts of cattle on the South American temperate forests: challenges for the conservation of the endangered monkey puzzle tree (Araucaria araucana) in Chile. Biol Conserv 152:110–118CrossRefGoogle Scholar
  82. Zawadzka D, Drozdowski S, Zawadzki G, Zawadzki J (2016) The availability of cavity trees along an age gradient in fresh pine forests. Silva Fennica 50:1441CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Instituto de Biología SubtropicalCONICET-Universidad Nacional de MisionesPuerto IguazúArgentina
  2. 2.Department of Forest and Conservation SciencesUniversity of British ColumbiaVancouverCanada
  3. 3.ECOS (Ecology-Complexity-Society) Laboratory, Centre for Local Development (CEDEL)Pontificia Universidad Católica de ChileVillaricaChile
  4. 4.Millennium Nucleus Centre for the Socioeconomic Impact of Environmental Policies (CESIEP) & Centre of Applied Ecology and Sustainability (CAPES)Pontificia Universidad Católica de ChileSantiagoChile
  5. 5.Science & Technology BranchEnvironment and Climate Change CanadaDeltaCanada

Personalised recommendations