Abstract
South American temperate rainforests, a global biodiversity hotspot, have been reduced to nearly 30% of their original extent and most remaining stands are being degraded. Cavity-nesting vertebrate communities are dependent on cavity-bearing trees and hierarchically structured within nest webs. Evaluating the actual degree of cavity dependence (obligate, non-obligate) and the preferred attributes of trees by cavity nesters is critical to design conservation strategies in areas undergoing habitat loss. During three breeding seasons (2010–2013), we studied the cavity-nesting bird community in temperate rainforests of Chile. We found the highest reported proportion of tree cavity nesters (n = 29 species; 57%) compared to non-cavity-using birds for any forest system. Four species were excavators and 25 were secondary cavity nesters (SCNs). Among SCNs, ten species were obligate and 15 were non-obligate cavity nesters. Seventy-five percent of nests of SCNs were located in cavities produced by tree decay processes and the remaining 25% were in cavities excavated mainly by Pygarrhichas albogularis and Campephilus magellanicus. Nest web structure had a low dominance and evenness, with most network interactions occurring between SCNs and large decaying trees. Tree diameter at breast height (DBH) was larger in nest-trees (57.3 cm) than in available trees (26.1 cm). Cavity nesters showed a strong preference for dead trees, both standing and fallen (58% of nests). Our results stress that retaining large decaying and standing dead trees (DBH > 57 cm), and large fallen trees, should be a priority for retention in forest management plans in this globally threatened ecosystem.
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11 November 2017
In the original publication of the article, Table 3 was incorrectly published. The corrected Table 3 is given below.
References
Aitken KEH, Martin K (2007) The importance of excavators in hole-nesting communities: availability and use of natural tree holes in old mixed forests of western Canada. J Ornithol 148:425–434. doi:10.1007/s10336-007-0166-9
Altamirano TA (2014) Breeding ecology of cavity-nesting birds in the Andean temperate forest of southern Chile. Pontificia Universidad Católica de Chile
Altamirano TA, Ibarra JT, Hernández F et al (2012) Hábitos de nidificación de las aves del bosque templado andino de Chile. Pontificia Universidad Católica de Chile, Santiago
Armesto J, Rozzi R, Smith-Ramirez C, Arroyo M (1998) Conservation targets in South American temperate forests. Science 282(80):1271–1272
Beaudoin F, Ojeda V (2011) Nesting of Rufous-legged owls in evergreen Nothofagus forests. J Raptor Res 45:75–77
Blakely TJ, Jellyman PG, Holdaway RJ et al (2008) The abundance, distribution and structural characteristics of tree-holes in Nothofagus forest, New Zealand. Austral Ecol 33:963–974. doi:10.1111/j.1442-9993.2008.01867.x
Blanc LA, Walters JR (2007) Cavity-nesting community webs as predictive tools: where do we go from here? J Ornithol 148:417–423. doi:10.1007/s10336-007-0232-3
Blanc L, Walters J (2008a) Cavity-nest webs in a longleaf pine ecosystem. Condor 110:80–92. doi:10.1525/cond.2008.110.1.80.80
Blanc L, Walters J (2008b) Cavity excavation and enlargement as mechanisms for indirect interactions in an avian community. Ecology 89:506–514
Boyle WA, Ganong CN, Clark DB, Hast MA (2008) Density, distribution, and attributes of tree cavities in an old-growth tropical rain forest. Biotropica 40:241–245. doi:10.1111/j.1744-7429.2007.00357.x
Bunnell FL, Kremsater LL, Wind E (1999) Managing to sustain vertebrate richness in forests of the Pacific Northwest: relationships within stands. Environ Rev 7:97–146. doi:10.1139/er-7-3-97
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Carmona M, Armesto J, Aravena J, Perez C (2002) Coarse woody debris biomass in successional and primary temperate forests in Chiloé Island, Chile. For Ecol Manag 164:265–275
Carneiro APB, Jiménez JE, Vergara PM, White TH (2013) Nest-site selection by slender-billed parakeets in a Chilean agricultural-forest mosaic. J F Ornithol 84:13–22. doi:10.1111/jofo.12001
Caviedes J, Ibarra JT (2017) Influence of anthropogenic disturbances on stand structural complexity in Andean temperate forests: implications for managing key habitat for biodiversity. PLoS ONE 12:e0169450. doi:10.1371/journal.pone.0169450
Cockle KL, Martin K, Wesołowski T (2011a) Woodpeckers, decay, and the future of cavity-nesting vertebrate communities worldwide. Front Ecol Environ 9:377–382. doi:10.1890/110013
Cockle KL, Martin K, Wiebe K (2011b) Selection of nest trees by cavity-nesting birds in the neotropical atlantic forest. Biotropica 43:228–236. doi:10.1111/j.1744-7429.2010.00661.x
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. doi:10.1016/j.foreco.2011.10.015
Cofre HL, Böhning-Gaese K, Marquet PA (2007) Rarity in Chilean forest birds: which ecological and life-history traits matter? Divers Distrib 13:203–212. doi:10.1111/j.1472-4642.2006.00312.x
CONAF (2014) Ley sobre recuperación del bosque nativo y fomento forestal y reglamentos. Ministerio de Agricultura, Gobierno de Chile, Santiago
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. doi:10.1111/j.2008.0030-1299.16215.x
Díaz S, Kitzberger T (2013) Nest habitat selection by the austral parakeet in north-western Patagonia. Austral Ecol 38:268–278. doi:10.1111/j.1442-9993.2012.02400.x
Díaz IA, Armesto JJ, Reid S et al (2005) Linking forest structure and composition: avian diversity in successional forests of Chiloé Island, Chile. Biol Conserv 123:91–101. doi:10.1016/j.biocon.2004.10.011
Dobkin D, Rich A, Pretare J, Pyle W (1995) Nest-site relationships among cavity-nesting birds of riparian and snowpocket aspen woodlands in the northwestern Great Basin. Condor 97:694–707
Drever MC, Martin K (2010) Response of woodpeckers to changes in forest health and harvest: implications for conservation of avian biodiversity. For Ecol Manag 259:958–966. doi:10.1016/j.foreco.2009.11.038
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. doi:10.1016/j.biocon.2007.12.004
Echeverria C, Coomes D, Salas J et al (2006) Rapid deforestation and fragmentation of Chilean temperate forests. Biol Conserv 130:481–494. doi:10.1016/j.biocon.2006.01.017
Edworthy AB, Martin K (2013) Persistence of tree cavities used by cavity-nesting vertebrates declines in harvested forests. J Wildl Manag 77:770–776. doi:10.1002/jwmg.526
Edworthy AB, Wiebe KL, Martin K (2012) Survival analysis of a critical resource for cavity-nesting communities: patterns of tree cavity longevity. Ecol Appl 22:1733–1742
Figueroa R, Corales E (2003) Notas sobre la conducta de crianza del Carpintero Bataraz Grande (Picoides lignarius) en el bosque lluvioso templado del sur de Chile. El Hornero 18:119–122
Fjeldså J, Krabbe N (1990) Birds of the high Andes. A manual to the birds of the temperate zone of the Andes and Patagonia, South America, 1st edn. Apollo Booksellers, London
Gibbons P, Lindenmayer D (2002) Tree hollows and wildlife conservation in Australia, 1st edn. CSIRO Publishing, Melbourne
Gibbons P, Lindenmayer D, Barry S, Tanton M (2002) Hollow selection by vertebrate fauna in forests of southeastern Australia and implications for forest management. Biol Conserv 103:1–12
Gibbs J, Hunter M, Melvin S (1993) Snag availability and communities of cavity nesting birds in tropical versus temperate forests. Biotropica 25:236–241
Goodall JP, Johnson AW, Philippi RA (1957) Las aves de Chile: su conocimiento y sus costumbres. Platt Establecimientos Gráficos, Buenos Aires
Huebner DP, Hurteau SR (2007) An economical wireless cavity-nest viewer. J Field Ornithol 78:87–92. doi:10.1111/j.1557-9263.2006.00089.x
Hurlbert S (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586
Ibarra JT, Martin K (2015a) Beyond species richness: an empirical test of top predators as surrogates for functional diversity and endemism. Ecosphere 6:1–15. doi:10.1890/es15-00207.1
Ibarra JT, Martin K (2015b) Biotic homogenization: loss of avian functional richness and habitat specialists in disturbed Andean temperate forests. Biol Conserv 192:418–427. doi:10.1016/j.biocon.2015.11.008
Jaksic F, Feinsinger P (1991) Bird assemblages in temperate forests of North and South America: a comparison of diversity, dynamics, guild structure, and resource use. Rev Chil Hist Nat 64:491–510
Jiménez JE, White TH (2011) Use of tree cavities for nesting by speckled teal (Anas flavirostris) in southern Chile: potential competition with the slender-billed parakeet (Enicognathus leptorhynchus). Ornitol Neotrop 22:465–469
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108. doi:10.1016/j.tree.2003.10.013
Jones J (2001) Habitat selection studies in avian ecology: a critical review. Auk 118:557–562
Koch AJ, Munks SA, Driscoll D, Kirkpatrick JB (2008a) Does hollow occurrence vary with forest type? A case study in wet and dry Eucalyptus obliqua forest. For Ecol Manag 255:3938–3951. doi:10.1016/j.foreco.2008.03.025
Koch AJ, Munks SA, Woehler EJ (2008b) Hollow-using vertebrate fauna of Tasmania: distribution, hollow requirements and conservation status. Aust J Zool 56:323–349
Lammertink M, Gallagher TW, Rosenberg KV et al (2011) Film documentation of the probably extinct imperial woodpecker (Campephilus imperialis). Auk 128:671–677. doi:10.1525/auk.2011.10271
Lindenmayer DB, Cunningham RB, Donnelly CF et al (1993) The abundance and development of cavities in Eucalyptus trees: a case study in the montane forests of Victoria, southeastern Australia. For Ecol Manag 60:77–104. doi:10.1016/0378-1127(93)90024-H
Lindenmayer DB, Laurance WF, Franklin JF et al (2014) New policies for old trees: averting a global crisis in a keystone ecological structure. Conserv Lett 7:61–69. doi:10.1111/conl.12013
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. doi:10.1016/S0378-1127(98)00403-4
Martin T, Geupel G (1993) Nest-monitoring plots: methods for locating nests and monitoring success. J Field Ornithol 64:507–519
Martin K, Aitken K, Wiebe K (2004) Nest sites and nest webs for cavity-nesting communities in interior British Columbia, Canada: nest characteristics and niche partitioning. Condor 106:5–19
Martínez D, González G (2004) Las aves de Chile, nueva guía de campo. Ediciones del Naturalista, Santiago
Müller J, Thorn S, Baier R et al (2016) Protecting the forests while allowing removal of damaged trees may imperil saproxylic insect biodiversity in the hyrcanian beech forests of Iran. Conserv Lett 9:106–113. doi:10.1111/conl.12187
Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. doi:10.1038/35002501
Newton I (1994) The role of nest sites in limiting the numbers of hole-nesting birds: a review. Biol Conserv 70:265–276. doi:10.1016/0006-3207(94)90172-4
Newton I (1998) Population limitation in birds, 1st edn. Academic Press, London
Ojeda V, Trejo A (2002) Primeros registros de nidificación en cavidades para tres especies de aves en el bosque andino patagónico. El Hornero 17:85–89
Ojeda VS, Suarez ML, Kitzberger T (2007) Crown dieback events as key processes creating cavity habitat for magellanic woodpeckers. Austral Ecol 32:436–445. doi:10.1111/j.1442-9993.2007.01705.x
Peña-Foxon M, Ippi S, Díaz I (2011) First nesting records of the endemic slender-billed parakeet (Enicognathus leptorhynchus) in southern Chile. Ornitol Neotrop 22:103–110
Pimm S, Raven P, Peterson A et al (2006) Human impacts on the rates of recent, present, and future bird extinctions. Proc Natl Acad Sci 103:10941–10946. doi:10.1073/pnas.0604181103
Politi N, Hunter M Jr, Rivera L (2009) Nest selection by cavity-nesting birds in subtropical montane forests of the Andes: implications for sustainable forest management. Biotropica 41:354–360. doi:10.1111/j.1744-7429.2008.00481.x
Politi N, Hunter M, Rivera L (2010) Availability of cavities for avian cavity nesters in selectively logged subtropical montane forests of the Andes. For Ecol Manag 260:893–906. doi:10.1016/j.foreco.2010.06.009
Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Core Team (2017) R: A language and environment for statistical computing. In: R Foundation Statistical Computing, Vienna. http://www.r-project.org/
Remm J, Lõhmus A (2011) Tree cavities in forests—the broad distribution pattern of a keystone structure for biodiversity. For Ecol Manage 262:579–585. doi:10.1016/j.foreco.2011.04.028
Ribeiro MT, Nunes F, Antonio F, Dos M (2009) Tree structure and richness in an Atlantic forest fragment: distance from anthropogenic and natural edges. Rev Árvore 33:1123–1132
Robles H, Ciudad C (2012) Influence of habitat quality, population size, patch size, and connectivity on patch-occupancy dynamics of the middle spotted woodpecker. Conserv Biol 26:284–293. doi:10.1111/j.1523-1739.2011.01816.x
Robles H, Martin K (2013) Resource quantity and quality determine the inter-specific associations between ecosystem engineers and resource users in a cavity-nest web. PLoS ONE 8:1–12. doi:10.1371/journal.pone.0074694
Rotheray GE, Hancock G, Hewitt S et al (2001) The biodiversity and conservation of Diptera in Scotland. J Insect Conserv 5:77–85
Rozzi R, Martínez D, Willson M, Sabag C (1996) Avifauna de los bosques templados de Sudamérica. In: Armesto J, Villagrán C, Arroyo M (eds) Ecología de los bosques nativos de Chile, 1st edn. Editorial Universitaria, Santiago, pp 135–152
Ruggera RA, Schaaf AA, Vivanco CG et al (2016) Exploring nest webs in more detail to improve forest management. For Ecol Manag 372:93–100. doi:10.1016/j.foreco.2016.04.010
Rybicki J, Hanski I (2013) Species-area relationships and extinctions caused by habitat loss and fragmentation. Ecol Lett 16:27–38. doi:10.1111/ele.12065
Sabatino M, Maceira N, Aizen MA (2010) Direct effects of habitat area on interaction diversity in pollination webs. Ecol Appl 20:1491–1497
Sedgwick J, Knopf F (1986) Cavity-nesting birds and the cavity-tree resource in plains cottonwood bottomlands. J Wildl Manag 50:247–252
Thomas JW, Anderson RG, Maser C, Bull EL (1979) Snags. In: Thomas JW (ed) Wildlife habitats in managed forests: the Blue Mountains of Oregon and Washington. Agriculture Handbook No. 553. USDA, Forest Service, Washington, DC, pp 60–77
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
Veblen TT, Kitzberger T, Lara A (1992) Disturbance and forest dynamics along a transect from Andean rain forest to patagonian shrubland. J Veg Sci 3:507–520. doi:10.2307/3235807
Vuilleumier F (1985) Forest birds of Patagonia: ecological geography, speciation, endemism, and faunal history. Ornithol Monogr 36:255–304
Wallace P (2010) Primer registro de nidificación de lechuza bataraz austral (Strix rufipes) en Argentina. Nuestras Aves 55:3
Wesołowski T, Martin KM (2017) Tree holes and hole nesting birds in European and North American forests. In: Mikusiński G, Roberge JM, Fuller RJ (eds) Ecology and conservation of forest birds, 1st edn. Ecology, biodiversity and conservation series. Cambridge Univ Press, Cambridge
Zarnowitz J, Manuwal D (1985) The effects of forest management on cavity-nesting birds in northwestern Washington. J Wildl Manag 49:255–263
Acknowledgements
We thank the financial support from the Chilean Ministry of the Environment (FPA Projects 09-083-08, 09-078-2010, 9-I-009-12), The Peregrine Fund, Environment Canada, Idea Wild Fund, Rufford Small Grants Foundation (14397-2), Neotropical Ornithological Society’s Francois Vuilleumier Fund for Research on Neotropical Birds, Vicerrectoría de Investigación from the Pontificia Universidad Católica de Chile (Internationalization Grant Agreement PUC1566-MINEDUC), “NETBIOAMERICAS” CONICYT/Apoyo a la Formación de Redes Internacionales entre Centros de Investigación (REDES150047), and CONICYT/FONDECYT de Inicio (11160932). We acknowledge the logistic support from the Chilean Forestry Service (CONAF). J. Laker (Kodkod: Lugar de Encuentros), M. Venegas and R. Sanhueza (Guías-Cañe), R. Timmerman, M. Sabugal, C. Délano, Lahuen Foundation, Kawellucó Private Sanctuary, and many landowners kindly allowed us to work on their properties. Special thanks to A. Vermehren, D. Cockle, M. de la Maza, M. T. Honorato, M. I. Mujica, and A. Dittborn for their great involvement on this project. Numerous friends and students provided invaluable assistance in the field. TAA is supported by a Postdoctoral scholarship from Comisión Nacional de Investigación Científica y Tecnológica (CONICYT).
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Communicated by Jan C. Habel.
This article belongs to the Topical Collection: Forest and plantation biodiversity.
A correction to this article is available online at https://doi.org/10.1007/s10531-017-1457-y.
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Altamirano, T.A., Ibarra, J.T., Martin, K. et al. 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 (2017). https://doi.org/10.1007/s10531-017-1369-x
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DOI: https://doi.org/10.1007/s10531-017-1369-x