Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated during the current study are available from the authors on reasonable request.

References

  • Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335:1486–1489

    Article  CAS  PubMed  Google Scholar 

  • 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:e0119952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 26:2453–2472

    Article  Google Scholar 

  • 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 367–390

    Chapter  Google Scholar 

  • Bai M-L, Wichmann F, Mühlenberg (2005) Nest-site characteristics of hole-nesting birds in a primeval boreal forest of Mongolia. Acta Ornithol 40:1–14

    Article  Google Scholar 

  • Blanc LA, Walters JR (2007) Cavity-nesting community webs as predictive tools: where do we go from here? J Ornithol 148(Suppl 2):S417–S423

    Article  Google Scholar 

  • Blanc LA, Walters JR (2008a) Cavity excavation and enlargement as mechanisms for indirect interactions in an avian community. Ecology 89:506–514

    Article  Google Scholar 

  • Blanc LA, Walters JR (2008b) Cavity-nest webs in a longleaf pine ecosystem. Condor 110:80–92

    Article  Google Scholar 

  • 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 32:41–64

    Google Scholar 

  • 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 84:13–22

    Article  Google Scholar 

  • Cockle KL, Martin K (2015) Temporal dynamics of a commensal network of cavity-nesting vertebrates: increased diversity during an insect outbreak. Ecology 96:1093–1104

    Article  Google Scholar 

  • 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 78:21–39

    Article  Google Scholar 

  • 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 143:2851–2857

    Article  Google Scholar 

  • Cockle K, Martin K, Wiebe K (2011a) Selection of nest trees by cavity-nesting birds in the Neotropical Atlantic forest. Biotropica 43:228–236

    Article  Google Scholar 

  • Cockle KL, Martin K, Wesołowski T (2011b) Woodpeckers, decay, and the future of cavity-nesting vertebrate communities worldwide. Front Ecol Environ 9:377–382

    Article  Google Scholar 

  • 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 264:210–219

    Article  Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • DeGraaf RM, Shigo AL (1985) Managing cavity trees for wildlife in the Northeast. US Forest Service Gen Tech Rep NE-101

  • 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 20:3055–3068

    Article  Google Scholar 

  • Díaz S, Kitzberger T (2013) Nest habitat selection by the austral parakeet in north-western Patagonia. Austral Ecol 38:268–278

    Article  Google Scholar 

  • Donoso C (1993) Bosques templados de Chile y Argentina: variación, estrutura y dinámica. Editorial Universitaria, Santiago

    Google Scholar 

  • Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite package: analysing ecological networks. R News 8(2):8–11

    Google Scholar 

  • Drever MC, Aitken KEH, Norris AR, Martin K (2008) Woodpeckers as reliable indicators of bird richness, forest health and harvest. Biol Conserv 141:624–634

    Article  Google Scholar 

  • 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:eaav6699

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang Y-T, Tuanmu M-N, Hung C-M (2018) Asynchronous evolution of interdependent nest characters across the avian phylogeny. Nat Commun 9:1863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galeano J, Pastor JM, Iriondo JM (2008) Weighted-Interaction Nestedness Estimator (WINE): a new estimator to calculate over frequency matrices. arXiv 0808.3397v2 [physics.bio-ph]

  • Gibbons P, Lindenmayer D (2002) Tree hollows and wildlife conservation in Australia. CSIRO, Collingwood

    Book  Google Scholar 

  • 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 35:597–615

    Article  Google Scholar 

  • Herrmann TM (2006) Indigenous knowledge and management of Araucaria araucana forest in the Chilean Andes: implications for native forest conservation. Biodivers Conserv 15:647–662

    Article  Google Scholar 

  • Hueck K (1972) As florestas da América do Sul. Editora da Universidade de Brasília/Editora Polígono, São Paulo

    Google Scholar 

  • Ibarra JT, Martin K (2015) Biotic homogenization: loss of avian functional richness and habitat specialists in disturbed Andean temperate forests. Biol Conserv 192:418–427

    Article  Google Scholar 

  • 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 20:33–45

    Google Scholar 

  • 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 7:4467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ilsøe SK, Kissling WD, Fjeldså JF, Sandel B, Svenning J-C (2017) Global variation in woodpecker species richness shaped by tree availability. J Biogeogr 44:1824–1835

    Article  Google Scholar 

  • IUCN (2018) The IUCN red list of threatened species. Version 2018-2. http://www.iucnredlist.org. Accessed 2 Dec 2018

  • 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 22:465–469

    Google Scholar 

  • Kershaw P, Wagstaff B (2001) The southern conifer family Araucariaceae: history, status, and value for paleoenvironmental reconstruction. Annu Rev Ecol Syst 32:397–414

    Article  Google Scholar 

  • 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 255:3938–3951

    Article  Google Scholar 

  • Lacerda AEB (2016) Conservation strategies for Araucaria forests in southern Brazil: assessing current and alternative approaches. Biotropica 48:537–544

    Article  Google Scholar 

  • 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 142:166–179

    Article  Google Scholar 

  • 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 39:235–252

    Article  Google Scholar 

  • Martin TE (2014) Consequences of habitat change and resource selection specialization for population limitation in cavity-nesting birds. J Appl Ecol 252:475–485

    Google Scholar 

  • Martin K, Eadie JM (1999) Nest webs: a community-wide approach to the management and conservation of cavity-nesting forest birds. For Ecol Manag 115:243–257

    Article  Google Scholar 

  • 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 106:5–19

    Article  Google Scholar 

  • Martín González AA, Dalsgaard B, Nogués-Bravo D et al (2015) The macroecology of phylogenetically structured hummingbird–plant networks. Glob Ecol Biogeogr 24:1212–1224

    Article  Google Scholar 

  • 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 22:672–681

    Article  Google Scholar 

  • 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 17:413–423

    Article  Google Scholar 

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717

    Article  PubMed  Google Scholar 

  • Millington WF, Chaney WR (1973) Shedding of shoots and branches. In: Kozlowski TT (ed) Shedding of plant parts. Physiological ecology. Academic Press, New York

    Google Scholar 

  • Monterrubio-Rico TC, Escalante-Pliego P (2006) Richness, distribution and conservation status of cavity-nesting birds in Mexico. Biol Conserv 128:67–78

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Norris AR, Martin K (2012) Red-breasted nuthatches (Sitta canadensis) increase cavity excavation in response to a mountain pine beetle (Dendroctonus ponderosae) outbreak. Ecoscience 19:308–315

    Article  Google Scholar 

  • Panti C, Pujana RR, Zamaloa MC, Romero EJ (2012) Araucariaceae macrofossil record from South America and Antarctica. Alcheringa 36:1–22

    Article  Google Scholar 

  • Pauchard A, Villarroel P (2002) Protected areas in Chile: history, current status, and challenges. Nat Areas J 22:318–330

    Google Scholar 

  • 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 21:3131–3155

    Article  Google Scholar 

  • 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 6:109–120

    Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Ragonese AE, Castiglioni JA (1946) Los pinares de Araucaria angustifolia en la República Argentina. Bol Soc Argent Bot 1:126–147

    Google Scholar 

  • 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 28:1867–1883

    Article  PubMed  Google Scholar 

  • 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 142:1141–1153

    Article  Google Scholar 

  • 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 20:193–206

    Google Scholar 

  • 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 8:7800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Cabal M, Nuñez M, Martínez AS (2008) Quantity versus quality: endemism and protected areas in the temperate forest of South America. Austral Ecol 33:730–736

    Article  Google Scholar 

  • Rother DC, Pizo MA, Jordano P (2016) Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages. Oikos 125:336–342

    Article  Google Scholar 

  • Ruggera RA, Schaaf AA, Vivanco CG, Politi N, Rivera LO (2016) Exploring nest webs in more detail to improve forest management. For Ecol Manag 372:93–100

    Article  Google Scholar 

  • 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, Brasília

    Google Scholar 

  • Sedrez dos Reis M, Ladio A, Peroni N (2014) Landscapes with Araucaria in South America: evidence for a cultural dimension. Ecol Soc 19:43

    Article  Google Scholar 

  • Sick H (1993) Birds in Brazil: a natural history. Princeton University Press, Princeton

    Google Scholar 

  • Soto GE, Vergara PM, Rodewald AD (2018) The fruit of competition: seed dispersal by Magellanic Woodpeckers in the threatened Valdivian Rainforest. Ecology 99:2617–2620

    Article  PubMed  Google Scholar 

  • 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 5:171456

    Article  PubMed  PubMed Central  Google Scholar 

  • Stotz DF, Fitzpatrick JW, Parker TA III, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press, Chicago

    Google Scholar 

  • 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 6:31709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:1–15

    Article  Google Scholar 

  • Trøjelsgaard K, Jordano P, Carstensen DW, Olesen JM (2015) Geographical variation in mutualistic networks: similarity, turnover and partner fidelity. Proc R Soc B 282:20142925

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279

    Article  Google Scholar 

  • 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 23:1120–1131

    Article  Google Scholar 

  • Veblen TT (1982) Regeneration patterns in Araucaria araucana forests in Chile. J Biogeogr 9:11–28

    Article  Google Scholar 

  • 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, Cambridge

    Google Scholar 

  • 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 8:3

    Article  Google Scholar 

  • 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 48:431–438

    Article  Google Scholar 

  • 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 152:110–118

    Article  Google Scholar 

  • Zawadzka D, Drozdowski S, Zawadzki G, Zawadzki J (2016) The availability of cavity trees along an age gradient in fresh pine forests. Silva Fennica 50:1441

    Article  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

  1. Instituto de Biología Subtropical, CONICET-Universidad Nacional de Misiones, Bertoni 85, 3370, Puerto Iguazú, Misiones, Argentina

    Kristina L. Cockle

  2. Department of Forest and Conservation Sciences, University of British Columbia, 2424 Main Mall, Vancouver, BC, V6T 1Z4, Canada

    Kristina L. Cockle, Tomás A. Altamirano & Kathy Martin

  3. ECOS (Ecology-Complexity-Society) Laboratory, Centre for Local Development (CEDEL), Pontificia Universidad Católica de Chile, Villarrica Campus, Villarica, Chile

    José Tomás Ibarra

  4. Millennium Nucleus Centre for the Socioeconomic Impact of Environmental Policies (CESIEP) & Centre of Applied Ecology and Sustainability (CAPES), Pontificia Universidad Católica de Chile, Santiago, Chile

    José Tomás Ibarra

  5. Science & Technology Branch, Environment and Climate Change Canada, 5421 Robertson Road, R. R. 1, Delta, BC, V4K 3N2, Canada

    Kathy Martin

Authors
  1. Kristina L. Cockle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Tomás Ibarra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomás A. Altamirano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kathy Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kristina L. Cockle.

Ethics declarations

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.

Additional information

Communicated by Karen E. Hodges.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article belongs to the Topical Collection: Forest and plantation biodiversity.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cockle, K.L., Ibarra, J.T., Altamirano, T.A. et al. Interspecific networks of cavity-nesting vertebrates reveal a critical role of broadleaf trees in endangered Araucaria mixed forests of South America. Biodivers Conserv 28, 3371–3386 (2019). https://doi.org/10.1007/s10531-019-01826-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-019-01826-4

Keywords

Search

Navigation