Bird species richness in High-Andean forest fragments: habitat quality and topography matter
DOI:
https://doi.org/10.26496/bjz.2020.76Keywords:
bird communities, conservation, exotic plantations, Polylepis, Tunari NPAbstract
Montane forests worldwide are known centers of endemism and biodiversity but are highly threatened by fragmentation processes. Using data collected in 15 Polylepis forest remnants covering 2000 hectares, we investigated how bird species richness and bird community composition, particularly for species of conservation concern, are influenced by habitat quality and topography in the Tunari National Park in the High Andes of Bolivia. Bird species richness was highest in topographically complex, low-elevation Polylepis patches located in areas with a high potential to retain rainwater. Bird communities differed strongly between Polylepis lanata and P. subtusalbida remnants, each supporting different threatened and endemic species. Within the P. subtusalbida forest, high-elevation fragments characterized by high amounts of sunlight and low anthropogenic disturbance were more likely to contain threatened species. Surprisingly, we found no effect of fragment size on the diversity or composition of bird communities or the presence of bird species of conservation concern. The presence of exotic plantations (Pinus and/or Eucalyptus spp.) in or outside forest remnants was negatively associated with the number of bird species as well as with occurrence of the endangered Cochabamba-mountain finch (Compsospiza garleppi). To support the different communities found in Polylepis forests, these results suggest that conservation efforts should be directed towards both forest types (P. subtusalbida and P. lanata) present in the area. For an efficient management of avian diversity, exotic plantations should be established away from native remnants while existing patches should be managed to maintain or increase habitat quality. Finally, the importance of local topography in determining avian species richness and community composition in forest fragments, mainly through topographic controls on moisture distribution and the amount of sunlight received by the fragments, should be considered when planning conservation and reforestation schemes.References
Alinari J., von Müller A. & Renison D. (2015). The contribution of fire damage to restricting high mountain Polylepis australis forests to ravines : Insights from an un-replicated comparison. Ecología Austral 25: 11–18.
Aubad J., Aragón P. & Rodríguez M.Á. (2010). Human access and landscape structure effects on Andean forest bird richness. Acta Oecologica 36 (4): 396–402. https://doi.org/10.1016/j.actao.2010.03.009
Azocar A., Rada F. & Garcia-Nunez C. (2007). Functional characteristics of the arborescent genus Polylepis along a latitudinal gradient in the high Andes. Interciencia 32 (10): 663–668.
Bader M.Y. & Ruijten J.J.A. (2008). A topography-based model of forest cover at the alpine tree line in the tropical Andes. Journal of Biogeography 35: 711–723. https://doi.org/10.1111/j.1365-2699.2007.01818.x
Balderrama J.A. (2006). Diversity, endemism and conservation issues of the avifauna of Tunari National Park (Cochabamba, Bolivia). Ecologia en Bolivia 41 (2): 149–170.
Balderrama J.A. (2009). Range extension for the endangered Cochabamba Mountain- Finch (Compsospiza garleppi) in Bolivia and new avifaunal records for Potosí department. Ecologia en Bolivia 44 (1): 67–69.
Barbosa K.V. de C., Knogge C., Develey P.F., Jenkins C.N. & Uezu A. (2017). Use of small Atlantic forest fragments by birds in Southeast Brazil. Perspectives in Ecology and Conservation 15 (1): 42–46. https://doi.org/10.1016/j.pecon.2016.11.001
Bartoń K. (2018). MuMIn, multi-model inference. R package version 1.42. 1.
Bellis L.M., Rivera L., Politi N., Martín E., Perasso M.L., Cornell F. & Renison D. (2009). Latitudinal patterns of bird richness, diversity and abundance in Polylepis australis mountain forest of Argentina. In: Bird Conservation International 19: 1–12. https://doi.org/10.1017/S0959270909008491
Bellis L.M., Pidgeon A.M., Alcántara C., Dardanelli S. & Radeloff V.C. (2015). Influences of succession and erosion on bird communities in a South American highland wooded landscape. Forest Ecology and Management 349: 85–93. https://doi.org/10.1016/j.foreco.2015.03.047
Besnard A.G., La Jeunesse I., Pays O. & Secondi J. (2013). Topographic wetness index predicts the occurrence of bird species in floodplains. Diversity and Distributions 19 (8): 955–963. https://doi.org/10.1111/ddi.12047
Beven K.J. & Kirkby M.J. (1979). A physically based, variable contributing area model of basin hydrology. Hydrological Sciences Bulletin 24 (1): 43–69. https://doi.org/10.1080/02626667909491834
BirdLife International (2012). Compsospiza garleppi. The IUCN Red List of Threatened Species 2012. https://doi.org/10.2305/IUCN.UK.2012-1.RLTS.T22723269A38110986.en
BirdLife International (2017). Important Bird Areas factsheet: Southern slopes of Tunari National Park (Vertiente Sur del Parque Nacional Tunari IBA). Available from http://datazone.birdlife.org/site/factsheet/southern-slopes-of-tunari-national-park-(vertiente-sur-del-parque-nacional-tunari-iba)-iba-bolivia/map [accessed 11 May 2017].
Brandt R., Zimmermann H., Hensen I., Mariscal Castro J.C. & Rist S. (2012). Agroforestry species of the Bolivian Andes: An integrated assessment of ecological, economic and socio-cultural plant values. Agroforestry Systems 86: 1–16. https://doi.org/10.1007/s10457-012-9503-y
Brose U., Martinez N.D. & Williams R.J. (2003). Estimating species richness: sensitivity to sample coverage and insensitivity to spatial patterns. Ecology 84 (9): 2364–2377.
Brugger S.O., Gobet E., Osmont D., Behling H., Fontana S.L., Hooghiemstra H., Morales-Molino C., Sigl M., Schwikowski M. & Tinner W. (2019). Tropical Andean glacier reveals colonial legacy in modern mountain ecosystems. Quaternary Science Reviews 220: 1–13. https://doi.org/10.1016/j.quascirev.2019.06.032
Burnham K.P. & Anderson D.R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (2nd edition). Springer, New York.
Bustamante R.O. & Simonetti J.A. (2005). Is Pinus radiata invading the native vegetation in Central Chile? Demographic responses in a fragmented forest. Biological Invasions 7: 243–249. https://doi.org/10.1007/s10530-004-0740-5
Cahill J.R.A. & Matthysen E. (2007). Habitat use by two specialist birds in high-Andean Polylepis forests. Biological Conservation 140 (1–2): 62–69. https://doi.org/10.1016/j.biocon.2007.07.022
Campos V.E., Cappa F.M., Viviana F.M. & Giannoni S.M. (2015). Using remotely sensed data to model suitable habitats for tree species in a desert environment. Journal of Vegetation Science 27 (1): 200–210. https://doi.org/10.1111/jvs.12328
Cavarzere V., Da Costa T.V.V. & Silveira L.F. (2012). On the use of 10-minute point counts and 10-species lists for surveying birds in lowland Atlantic forests in southeastern Brazil. Papéis Avulsos de Zoologia 52 (28): 333–341. https://doi.org/10.1590/S0031-10492012002800001
Cayuela L., Golicher D.J., Benayas J.M.R., González-Espinosa M. & Ramírez-Marcial N. (2006). Fragmentation, disturbance and tree diversity conservation in tropical montane forests. Journal of Applied Ecology 43 (6): 1172–1181. https://doi.org/10.1111/j.1365-2664.2006.01217.x
Chevallier P., Pouyaud B., Suarez W. & Condom T. (2011). Climate change threats to environment in the tropical Andes: glaciers and water resources. Regional Environmental Change 11: 179–187. https://doi.org/10.1007/s10113-010-0177-6
Cierjacks A., Rühr N.K., Wesche K. & Hensen I. (2007). Effects of altitude and livestock on the regeneration of two tree line forming Polylepis species in Ecuador. Plant Ecology 194 (2): 207–221. https://doi.org/10.1007/s11258-007-9285-x
Colwell R.K., Chao A., Gotelli N.J., Lin S.Y., Mao C.X., Chazdon R.L. & Longino J.T. (2012). Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology 5 (1): 3–21. https://doi.org/10.1093/jpe/rtr044
De Coster G., Matthysen E., Cahill J.R.A. & Lens L. (2009). Home range characteristics of the Near Threatened Giant Conebill Oreomanes fraseri in fragmented Polylepis forest. Bird Conservation International 19: 215–223. https://doi.org/10.1017/S0959270909008302
De la Hera I., Arizaga J. & Galarza A. (2013). Exotic tree plantations and avian conservation in northern Iberia: a view from a nest-box monitoring study. Animal Biodiversity and Conservation 36 (2): 153–163.
Doumenge C., Gilmour D., Ruiz Perez M. & Blockhus J. (1995). Tropical montane cloud forests: conservation status and management issues. In: Hamilton L.S., Juvik J.O. & Scatena F.N. (eds) Tropical Montane Cloud Forests. Ecological Studies (Analysis and Synthesis) 110: 24–37. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2500-3_2
Dray S. & Dufour A.B. (2007). The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22 (4): 1–20. https://doi.org/10.18637/jss.v022.i04
Dunford W. & Freemark K. (2005). Matrix matters: effects of surrounding land uses on forest birds near Ottawa, Canada. Landscape Ecology 20 (5): 497–511. https://doi.org/10.1007/s10980-004-5650-5
Estades C.F. & Temple S.A. (1999). Deciduous-forest bird communities in a fragmented landscape dominated by exotic pine plantations. Ecological Applications 9 (2): 573–585. https://doi.org/10.1890/1051-0761(1999)009[0573:DFBCIA]2.0.CO;2
FAUNAGUA (2015). Plan de manejo Parque Nacional Tunari - Caracterizacion integral de la fauna y propuesta de zonificacion específica.
Fjeldså J. (1993). The avifauna of the Polylepis woodlands of the Andean highlands: the efficiency of basing conservation priorities on patterns of endemism. Bird Conservation International 3: 37–55. https://doi.org/10.1017/S0959270900000770
Fjeldså J. (2002). Key areas for conserving the avifauna of Polylepis forests. Ecotropica 8: 125–131.
Fjeldså J. & Kessler M. (1996). Conserving the Biological Diversity of Polylepis Woodlands of the Highland of Peru and Bolivia. A Contribution to Sustainable Natural Resource Management in the Andes. Centre for Tropical Biodiversity, Copenhagen.
Flaspohler D.J., Giardina C.P., Asner G.P., Hart P., Price J., Lyons C.K. & Castaneda X. (2010). Long-term effects of fragmentation and fragment properties on bird species richness in Hawaiian forests. Biological Conservation 143 (2): 280–288. https://doi.org/10.1016/j.biocon.2009.10.009
Gareca E.E., Martinez Y.Y., Bustamante R.O., Aguirre L.F. & Siles M.M. (2007). Regeneration patterns of Polylepis subtusalbida growing with the exotic trees Pinus radiata and Eucalyptus globulus at Parque Nacional Tunari, Bolivia. Plant Ecology 193 (2): 253–263. https://doi.org/10.1007/s11258-007-9263-3
Gareca E.E., Fjeldså J., Honnay O. & Hermy M. (2010). Polylepis woodland remnants as biodiversity islands in the Bolivian high Andes. Biodiversity and Conservation 19 (12): 3327–3346. https://doi.org/10.1007/s10531-010-9895-9
Gosling W.D., Hanselman J.A., Knox C., Valencia B.G. & Bush M.B. (2009). Long-term drivers of change in Polylepis woodland distribution in the central Andes. Journal of Vegetation Science 20: 1041–1052. https://doi.org/10.1111/j.1654-1103.2009.01102.x
Gotelli N.J. & Colwell R.K. (2001). Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4 (4): 379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
Hanski I. (1998). Metapopulation dynamics. Nature 396 (6706): 41–49. https://doi.org/10.1038/23876
Hanski I. & Ovaskainen O. (2002). Extinction debt at extinction threshold. Conservation Biology 16 (3): 666–673. https://doi.org/10.1046/j.1523-1739.2002.00342.x
Heinze G., Ploner M., Dunkler D. & Southworth H. (2013). logistf: Firth’s Bias Reduced Logistic Regression. R package version 1.23. Available from http://cran.r-project.org/package=logistf [accessed 15 July 2020].
Hensen I. (2002). Impacts of anthropogenic activity on the vegetation of Polylepis woodlands in the region of Cochabamba, Bolivia. Ecotropica 8: 183–203.
Hensen I., Cierjacks A., Hirsch H., Kessler M., Romoleroux K., Renison D. & Wesche K. (2012). Historic and recent fragmentation coupled with altitude affect the genetic population structure of one of the world’s highest tropical tree line species. Global Ecology and Biogeography 21: 455–464. https://doi.org/10.1111/j.1466-8238.2011.00691.x
Herzog S.K., Kessler M. & Cahill T. (2002). Estimating species richness of tropical bird communities from rapid assessment data. The Auk 119 (3): 749–769. https://doi.org/10.1642/0004-8038(2002)119[0749:ESROTB]2.0.CO;2
Hjarsen T. (1998). Biological diversity in high altitude woodlands and plantations in the bolivian Andes: implications for development of sustainable land-use. In: Sarmiento F.H.O. & Hidalgo A.J. (eds) III Simposio Internacional de Desarollo Sustentable de Montañas: entiendo las interfaces ecológicas para la gestión de los paisajes culturales en los Andes: 145–149. Corporación Editora Nacional, Quito, Ecuador.
Homeier J., Breckle S.-W., Günter S., Rollenbeck R.T. & Leuschner C. (2010). Tree diversity, forest structure and productivity along altitudinal and topographical gradients in a species-rich Ecuadorian montane rain forest. Biotropica 42 (2): 140–148. https://doi.org/10.1111/j.1744-7429.2009.00547.x
Huanca E., Hosner P.A. & Hennessey A.B. (2009). Nests, vocalizations, and conservation status of endangered Cochabamba Mountain-Finches (Compospiza garleppi). Journal of Field Ornithology 80 (3): 215–223. https://doi.org/10.1111/j.1557-9263.2009.00224.x
Hurlbert A.H. & Haskell J.P. (2003). The effect of energy and seasonality on avian species richness and community composition. The American Naturalist 161 (1): 83–97.
IUCN (2018). The IUCN Red List of Threatened Species. Available from http://www.iucnredlist.org [accessed 25 October 2018].
Kattan G.H., Franco P., Saavedra-Rodríguez C.A., Valderrama C., Rojas V., Osorio D. & Martínez J. (2006). Spatial components of bird diversity in the Andes of Colombia: Implications for designing a regional reserve system. Conservation Biology 20 (4): 1203–1211.
https://doi.org/10.1111/j.1523-1739.2006.00402.x
Kessler M. & Schmidt-Lebuhn A.N. (2006). Taxonomical and distributional notes on Polylepis (Rosaceae). Organisms, Diversity & Evolution 6 (1): 67–69. https://doi.org/10.1016/j.ode.2005.04.001
Lloyd H. (2008a). Influence of within-patch habitat quality on high-Andean Polylepis bird abundance. Ibis 150 (4): 735–745. https://doi.org/10.1111/j.1474-919X.2008.00843.x
Lloyd H. (2008b). Abundance and patterns of rarity of Polylepis birds in the Cordillera Vilcanota, southern Perú: implications for habitat management strategies. Bird Conservation International 18 (2): 164–180. https://doi.org/10.1017/S0959270908000166
Lloyd H. & Marsden S.J. (2008). Bird community variation across Polylepis woodland fragments and matrix habitats: implications for biodiversity conservation within a high Andean landscape. Biodiversity and Conservation 17 (11): 2645–2660. https://doi.org/10.1007/s10531-008-9343-2
Lloyd H. & Marsden S.J. (2011). Between-patch bird movements within a high-Andean Polylepis woodland/matrix Llandscape: implications for habitat restoration. Restoration Ecology 19 (1): 74–82. https://doi.org/10.1111/j.1526-100X.2009.00542.x
MacKinnon J. & Phillips K. (1993). A Field Guide to the Birds of Borneo, Sumatra, Java and Bali: the Greater Sunda Islands. Oxford University Press, Oxford.
Macleod R., Ewing S.K., Herzog S.K., Bryce R., Evans K.L. & Maccormick A. (2006). First ornithological inventory and conservation assessment for the yungas forests of the Cordilleras Cocapata and Mosetenes, Cochabamba, Bolivia. Bird Conservation International 15 (4): 361. https://doi.org/10.1017/S095927090500064X
MacLeod R., Herzog S.K., Maccormick A., Ewing S.R., Bryce R. & Evans K.L. (2011). Rapid monitoring of species abundance for biodiversity conservation: consistency and reliability of the MacKinnon lists technique. Biological Conservation 144 (5): 1374–1381. https://doi.org/10.1016/j.biocon.2010.12.008
Marcora P.I., Renison D., País-Bosch A.I., Cabido M.R. & Tecco P.A. (2013). The effect of altitude and grazing on seedling establishment of woody species in central Argentina. Forest Ecology and Management 291: 300–307. https://doi.org/10.1016/j.foreco.2012.11.030
Martínez-Morales M.A. (2005). Landscape patterns influencing bird assemblages in a fragmented neotropical cloud forest. Biological Conservation 121 (1): 117–126. https://doi.org/10.1016/j.biocon.2004.04.015
Mortelliti A. & Lindenmayer D.B. (2015). Effects of landscape transformation on bird colonization and extinction patterns in a large-scale, long-term natural experiment. Conservation Biology 29 (5): 1314–1326. https://doi.org/10.1111/cobi.12523
Navarro G., Molina J.A. & De la Barra N. (2005). Classification of the high-Andean Polylepis forests in Bolivia. Plant Ecology 176 (1): 113–130. https://doi.org/10.1007/s11258-004-0025-1
O’Dea N., Watson J.E.M. & Whittaker R.J. (2004). Rapid assessment in conservation research: a critique of avifaunal assessment techniques illustrated by Ecuadorian and Madagascan case study data. Diversity and Distributions 10 (1): 55–63. https://doi.org/10.1111/j.1472-4642.2004.00050.x
Oksanen J., Blanchet F.G., Friendly M., Kindt R., Legendre P., Mcglinn D., Minchin P.R., O’hara R.B., Simpson G.L., Solymos P., Henry M., Stevens H., Szoecs E. & Maintainer H.W. (2019). Package ‘vegan’ – CRAN. Title Community Ecology Package Version 2.5-6.
Poulsen B.O., Krabbe N., Frølander A., Hinojosa M.B. & Quiroga C.O. (1997). A rapid assessment of Bolivian and Ecuadorian montane avifaunas using 20-species lists: efficiency, biases and data gathered. Bird Conservation International 7 (1): 53–67. https://doi.org/10.1017/S0959270900001404
Prevedello J.A. & Vieira M.V. (2010). Does the type of matrix matter? A quantitative review of the evidence. Biodiversity and Conservation 19 (5): 1205–1223. https://doi.org/10.1007/s10531-009-9750-z
Purcell J., Brelsford A. & Kessler M. (2002). The World’ s Highest Forest. A better understanding of the properties of Andean queñua woodlands has major implications for their conservation. American Scientist 92: 454–461.
R Development Core Team (2008). R: A language and environment for statistical computing. Vienna, Austria. Available from http://www.r-project.org [accessed 16 July 2020].
Renison D., Hensen I., Suarez R., Cingolani A.M., Marcora P. & Giorgis M.A. (2010). Soil conservation in Polylepis mountain forests of Central Argentina: Is livestock reducing our natural capital? Austral Ecology 35: 435–443. Available from https://doi.org/10.1111/j.1442-9993.2009.02055.x [accessed 16 July 2020].
Renison D., Hensen I. & Suarez R. (2011). Landscape structural complexity of high-mountain Polylepis australis forests: a new aspect of restoration goals. Restoration Ecology 19 (3): 390–398. https://doi.org/10.1111/j.1526-100X.2009.00555.x
Sanabria Siles N., Auza Aramayo M., Dalence Martinic J., Herrera B. & Avilés Ribera S. (2012). Aptitud de aprovechamiento sostenible y de conservación del parque nacional Tunari. Self published, Cercado, Bolivia.
SERNAP (2016). Parque Nacional Tunari: Información general. Available from http://www.sernap.gob.bo/index.php?option=com_content&view=article&id=82&Itemid=285 [accessed 6 June 2016].
Sevillano-Ríos C.S. & Rodewald A.D. (2017). Avian community structure and habitat use of Polylepis forests along an elevation gradient. PeerJ 5: e3220. https://doi.org/10.7717/peerj.3220
Sevillano Ríos S., Lloyd H. & Valdés-Velásquez A. (2011). Bird species richness, diversity and abundance in Polylepis woodlands, Huascaran biosphere reserve, Peru. Studies on Neotropical Fauna and Environment 46 (1): 69–76. https://doi.org/10.1080/01650521.2010.546567
Sparacino J., Renison D., Devegili A.M. & Suarez R. (2019). Wind protection rather than soil water availability contributes to the restriction of high-mountain forest to ravines. New Forests 51: 101–117. https://doi.org/10.1007/s11056-019-09722-z
Sylvester S.P., Sylvester M.D.P.V. & Kessler M. (2014). Inaccessible ledges as refuges for the natural vegetation of the high Andes. Journal of Vegetation Science 25: 1225–1234. https://doi.org/10.1111/jvs.12176
Tarboton D.G. (2009). TauDEM (Terrain Analysis Using Digital Elevation Models) Package. Available from http://hydrology.neng.usu.edu/taudem [accessed 27 July 2020].
Tinoco B.A., Astudillo P.X., Latta S.C., Strubbe D. & Graham C.H. (2013). Influence of patch factors and connectivity on the avifauna of fragmented Polylepis forest in the Ecuadorian Andes. Biotropica 45 (5): 602–611. https://doi.org/10.1111/btp.12047
Toivonen J.M., Kessler M., Ruokolainen K. & Hertel D. (2011). Accessibility predicts structural variation of Andean Polylepis forests. Biodiversity and Conservation 20 (8): 1789–1802. https://doi.org/10.1007/s10531-011-0061-9
Toivonen J.M., Gonzales-Inca C.A., Bader M.Y., Ruokolainen K. & Kessler M. (2018). Elevational shifts in the topographic position of Polylepis forest stands in the Andes of southern Peru. Forests 9 (7): 1–10. https://doi.org/10.3390/f9010007
Torres R.C., Renison D., Hensen I., Suarez R. & Enrico L. (2008). Polylepis australis’ regeneration niche in relation to seed dispersal, site characteristics and livestock density. Forest Ecology and Management 254: 255–260. https://doi.org/10.1016/j.foreco.2007.08.007
Weiss A. (2001). Topographic Position and Landforms Analysis. Band 64. Poster presentation, ESRI User Conference, San Diego, CA. Available from http://www.jennessent.com/downloads/TPI-poster-TNC_18x22.pdf [accessed 16 July 2020].
Wethered R. & Lawes M.J. (2003). Matrix effects on bird assemblages in fragmented Afromontane forests in South Africa. Biological Conservation 114 (3): 327–340. https://doi.org/10.1016/S0006-3207(03)00052-1
Williams J.J., Gosling W.D., Coe A.L., Brooks S.J. & Gulliver P. (2011). Four thousand years of environmental change and human activity in the Cochabamba Basin, Bolivia. Quaternary Research 76: 58–68. https://doi.org/10.1016/j.yqres.2011.03.004
Wilson J.W., Sexton J.O., Todd Jobe R. & Haddad N.M. (2013). The relative contribution of terrain, land cover, and vegetation structure indices to species distribution models. Biological Conservation 164: 170–176. https://doi.org/10.1016/j.biocon.2013.04.021
World Conservation Monitoring Centre (WCMC) (1998). Polylepis besseri ssp. subtusalbida. The IUCN Red List of Threatened Species.
https://doi.org/10.2305/IUCN.UK.1998.RLTS.T37147A10036721.en
Zurita G.A., Rey N., Varela D.M., Villagra M. & Bellocq M.I. (2006). Conversion of the Atlantic Forest into native and exotic tree plantations: effects on bird communities from the local and regional perspectives. Forest Ecology and Management 235: 164–173. https://doi.org/10.1016/j.foreco.2006.08.009
Downloads
Published
How to Cite
Issue
Section
License
All published papers will be put on-line as high resolution PDF’s. Copyright thus remains with the authors. All manuscripts will be licensed under a Creative Commons Attribution 3.0 License https://creativecommons.org/licenses/by/4.0/.