Habitat heterogeneity rather than the limits of protected areas influence bird communities in an Andean biosphere reserve
DOI:
https://doi.org/10.25260/EA.20.30.3.0.1068Keywords:
páramo grassland, Macizo del Cajas Biosphere Reserve, elevation, trophic guilds, specialist birdsAbstract
The páramo ecosystem harbors a high concentration of restricted range and threatened bird species. However, human modifications to the high Andean landscape have generated habitat loss and fragmentation throughout this ecosystem. Therefore, protected areas in this region are a priority for biodiversity conservation. Buffer zones around protected areas aim to reduce perturbation within them. However, these areas are still not exempt from sources of stress. We used abundance and diversity of birds, recorded by walking transects, in order to compare the community composition occurring in protected areas and adjacent buffer zones in a hotspot of diversity and endemism: the Macizo del Cajas Biosphere Reserve, in the southern high-Andes of Ecuador. The bird community did not vary in its composition between protected areas and buffer zones. However, the habitat characteristics explained differences in the presence and abundance of trophic guilds. Particularly, increasingly heterogeneous páramo grassland with greater woody plant cover and less intervention explained a greater presence and abundance of more specialized trophic guilds such as nectarivores in shrubs and aerial insectivores in trees and shrubs. We conclude that there are heterogeneous páramo habitats in buffer zones that should be considered in more formal conservation planning to maintain the diversity of specialized birds and therefore functionality of the páramo grassland ecosystem.
References
Aguilar, J. M., A. Nieto, N. Espinoza, G. Loja, and B. A. Tinoco. 2019. Assessing patterns of bird roadkills in a high Andean Ecuadorian national park. Studies on Neotropical Fauna and Environment 0:1-8. https://doi.org/10.1080/01650521.2019.1649953.
Armenteras, D., F. Gast, and H. Villareal. 2003. Andean Forest Fragmentation and the Representativeness of Protected Natural Areas in the Eastern Andes, Colombia. Biological Conservation 113(2):245-56. https://doi.org/10.1016/S0006-3207(02)00359-2.
Astudillo, P. X., B. A. Tinoco, and D. S. Siddons. 2015. The avifauna of Cajas National Park and Mazán Reserve, southern Ecuador, with notes on new records. Cotinga 37:1-11.
Astudillo, P. X., S. Barros, D. S. Siddons, and E. Zárate. 2017. Influence of habitat modification by livestock on páramo bird abundance in southern Andes of Ecuador. Studies on Neotropical Fauna and Environment 53(1):29-37. https://doi.org/10.1080/01650521.2017.1382122.
Astudillo, P. X., D. G. Schabo, D. C. Siddons, and N. Farwig. 2019. Patch-matrix movements of birds in the páramo landscape of the southern Andes of Ecuador. Emu-Austral Ornithology 119(1):53-60. https://doi.org/10.1080/01584197.2018.1512371.
Astudillo, P. X., I. Grass, D. C. Siddons, D. G. Schabo, and N. Farwig. 2020. Centrality in Species-Habitat Networks Reveals the Importance of Habitat Quality for High-Andean Birds in Polylepis Woodlands. Ardeola 67(2):307. https://doi.org/10.13157/arla.67.2.2020.ra5.
Baquero, F., R. Sierra, L. Ordóñez, M. Tipán, L. Espinosa, M. Rivera, and P. Soria. 2004. La Vegetación De Los Andes Del Ecuador. EcoCiencia, CESLA, Corporación EcoPar, MAG SIGAGRO, CDC Jatun Sacha, División Geográfica-IGM. Quito, Ecuador.
Benham, P. M., E. J. Beckman, S. G. DuBay, L. M. Flores, A. B. Johnson, M. J. Lelevier, C. J. Schmitt, N. A. Wright, and C. C. Witt. 2011. Satellite imagery reveals new critical habitat for endangered bird species in the high Andes of Peru. Endangered Species Research 13:145-157. https://doi.org/10.3354/esr00323.
Bucheli, G. F. 2007. Parque Nacional Cajas una oportunidad para la vida y el desarrollo local sustentable. Cuenca (Ecuador): Empresa Municipal de Telecomunicaciones, Agua Potable, Alcantarillado y Saneamiento Ambiental de Cuenca.
Carvalho Perelló, L. F., D. L. Guadagnin, L. Maltchik, and J. E. dos Santos. 2012. Ecological, legal, and methodological principles for planning buffer zones. Natureza and Conservação 10(1):3-11. http://doi.org/10.4322/natcon.2012.002.
Castaño-Villa, G. J. 2005. Áreas protegidas, criterios para su selección y problemáticas en su conservación. Boletín Científico, Centro de Museos, Museo de Historia Natural 10:79-102.
Celleri, R., P. Willems, W. Buytaert, and J. Feyen. 2007. Space-time rainfall variability in the Paute basin, Ecuadorian Andes. Hydrological Processes: An International Journal 21:3316-3327. https://doi.org/10.1002/hyp.6575.
DeFries, R., A. Hansen, A. C. Newton, and M. C. Hansen. 2005. Increasing isolation of protected areas in tropical forests over the past twenty years. Ecological Applications 15:19-26. https://doi.org/10.1890/03-5258.
Delgado, O., F. López, M. Aguilar, and M. Cordero. 2006. Componente geomorfología glaciar del Parque Nacional Cajas - Ecuador. In Press. Cuenca: Universidad del Azuay y Parque Nacional Cajas.
Fjeldså, J., and N. Krabbe. 1990. Birds of the High Andes. Zoological Museum, University of Copenhagen and Apollo Books, Svendborg, Denmark.
Foley, J. A., R. Defries, G. P. Asner, C. Barford, G. Bonan, S. R. Carpenter, and P. K. Snyder. 2005. Global consequences of land use. Science 309:570-574. https://doi.org/10.1126/science.1111772.
Grass, I., D. G. Berens, and N. Farwig. 2013. Guild-specific shifts in visitation rates of frugivores with habitat loss and plant invasion. Oikos 123:575-582. https://doi.org/10.1111/j.1600-0706.2013.00920.x.
Gray, C. L., S. L. Hill, T. Newbold, L. N. Hudson, L. Börger, S. Contu, A. J. Hoskins, S. Ferrier, A. Purvis, and J. P. Scharlemann. 2016. Local biodiversity is higher inside than outside terrestrial protected areas worldwide. Nature Communications 7(1):1-7. https://doi.org/10.1038/ncomms12306.
Hamer, T. L., C. H. Flather, and B. R. Noon. 2006. Factors associated with grassland bird species richness: the relative roles of grassland area, landscape structure, and prey. Landscape Ecology 21:569-583. https://doi.org/10.1007/s10980-005-2167-5.
Hansen, A. J., and J. Rotella. 2002. Biophysical factors, land use, and species viability in and around nature reserves. Conservation Biology 16:1112-1122. https://doi.org/10.1046/j.1523-1739.2002.00545.x.
Hansen, A. J., and R. DeFries. 2007. Ecological mechanisms linking protected areas to surrounding lands. Ecological Applications 17:974-988. https://doi.org/10.1890/05-1098.
Harden, C., and A. L. Borrero. 2005. Report on the geomorphology of Parque Nacional Cajas. In press. Cuenca: Parque Nacional Cajas.
Haslem, A., and A. F. Bennett. 2008. Birds in agricultural mosaics: the influence of landscape pattern and countryside heterogeneity. Ecological Applications 18:185-196. https://doi.org/10.1890/07-0692.1.
Hofstede, R., R. P. Coppus, P. M. Vásconez, P. Segarra, J. Wolf, and J. Sevink. 2002. El estado de conservación de los páramos de pajonal en el Ecuador. Ecotropicos 15:3-18.
Hooper, D. U., E. C. Adair, B. J. Cardinale, J. E. Byrnes, B. A. Hungate, K. L. Matulich, A. González, J. E. Duffy, L. Gamfeldt, and M. L. O’Connor. 2012. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105-108. https://doi.org/10.1038/nature11118.
Jackson, D. A. 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204-2214. https://doi.org/10.2307/1939574.
Jiménez-Rivillas, C., J. J. García, M. A. Quijano-Abril, J. M. Daza, and J. J. Morrone. 2018. A new biogeographical regionalisation of the Páramo biogeographic province. Australian systematic botany 31:296-310. https://doi.org/10.1071/SB18008.
Jørgensen, P., C. Ulloa-Ulloa, B. León, S. León-Yánez, S. Beck, M. Nee, J. Zarucchi, M. Celis, R. Bernal, and R. Gradstein. 2011. Regional patterns of vascular plant diversity and endemism. Pp. 192-203 in S. K. Herzog, R. Martínez, P. Jørgensen and H. Tiess (eds.). Climate change and biodiversity in the tropical Andes. São José dos Campos (Brazil): Inter-American Institute for Global Change Research (IAI) and Scientific Committee on Problems of the Environment (SCOPE).
Koenen, M. T., and S. G. Koenen. 2000. Effects of fire on birds in Paramo habitat of northern Ecuador. Ornitologia Neotropical 11:155-163.
Latta, S. C., B. A. Tinoco, and C. H. Graham. 2011. Patterns and Magnitude of Temporal Change in Avian Communities in the Ecuadorian Andes. The Condor 113:24-40. https://doi.org/10.1525/cond.2011.090252.
Laurance, W. F., J. Sayer, and K. G. Cassman. 2014. Agricultural expansion and its impacts on tropical nature. Trends in Ecology and Evolution 29:1-10. https://doi.org/10.1016/j.tree.2013.12.001.
Lazo, P. X., G. M. Mosquera, J. J. McDonnell, and P. Crespo. 2019. The Role of Vegetation, Soils, and Precipitation on Water Storage and Hydrological Services in Andean Páramo Catchments. Journal of Hydrology 572:805-19. https://doi.org/10.1016/j.jhydrol.2019.03.050.
Lloyd, H., and S. J. Marsden. 2008. Bird community variation across Polylepis woodland fragments and matrix habitats: implications for biodiversity conservation within a high Andean landscape. Biodiversity and Conservation 17:2645-2660. https://doi.org/10.1007/s10531-008-9343-2.
Lloyd, H., and S. J. Marsden. 2011. Between-Patch Bird Movements within a High-Andean Polylepis Woodland/Matrix Landscape: Implications for Habitat Restoration. Restoration Ecology 19:74-82. https://doi.org/10.1111/j.1526-100X.2009.00542.x.
Margules, C. R., and R. L. Pressey. 2000. Systematic conservation planning. Nature 405:243-253. https://doi.org/10.1038/35012251.
Matson, E., and D. Bart. 2013. Interactions among fire legacies, grazing and topography predict shrub encroachment in post-agricultural páramo. Landscape Ecology 28:1829-1840. https://doi.org/10.1007/s10980-013-9926-5.
McKinney, M. L., and J. L. Lockwood. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution 14:450-453. https://doi.org/10.1016/S0169-5347(99)01679-1.
Mena-Vásconez, P., and R. Hofstede. 2006. Los páramos ecuatorianos. Pp. 91-109 in M. Morales, B. Øllgaard, L. P. Vist, F. Borchsenius and H. Balslev (eds.). Botánica Económica de los Andes Centrales. La Paz: Universidad Mayor de San Andrés.
Minga, D., and A. Verdugo. 2007. Riqueza florística y endemismo del Parque Nacional Cajas. Herbario Azuay. Universidad del Azuay, Cuenca Ecuador.
Minga, D., A. Verdugo, R. Ansaloni, and J. Izco. 2013. Diversidad fitocenótica en el Parque Nacional Cajas. Universidad del Azuay, Cuenca, Ecuador.
Minga, D., R. Ansaloni, A. Verdugo, and C. Ulloa. 2016. Flora del páramo del Cajas, Ecuador. Cuenca, Bachelor’s thesis, Universidad del Azuay.
Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. Da Fonseca, and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-8. https://doi.org/10.1038/35002501.
Neill, D. A. 1999. Vegetación. Pp. 13-25 in P. M. Jørgensen and S. León-Yánez (eds.). Catalogue of Vascular plants of Ecuador. Vol. 75. St. Louis (MO): Monographs in Systematic Botany from the Missouri Botanical Garden.
Neuschulz, E., M. Brown, and N. Farwig. 2013. Frequent bird movements across a highly fragmented landscape: the role of species traits and forest matrix. Animal Conservation 16:170-179. https://doi.org/10.1111/j.1469-1795.2012.00582.x.
Norment, C. J., M. C. Runge, and M. R. Morgan. 2010. Breeding biology of Grassland Birds in Western New York: conservation and management implications. Avian Conservation and Ecology 5:1-14. https://doi.org/10.5751/ACE-00399-050203.
Nur, N., S. L. Jones, and G. R. Geupel. 1999. A statistical guide to data analysis of avian monitoring programs. U.S. Department of the Interior, Fish and Wildlife Service, Washington, D.C.
O’Dea, N., M. B. Araujo, and R. J. Whittaker. 2006. How Well Do Important Bird Areas Represent Species and Minimize Conservation Conflict in the Tropical Andes? Diversity and Distributions 12(2):205-14. https://doi.org/10.1111/j.1366-9516.2006.00235.x.
Oksanen, J., F. Guillaume Blanchet, R. Kindt, P. Legendre, D. Mcglinn, P. R. Minchin, R. B. O’hara, G. L. Simpson, P. Solymos, M. H. Stevens, E. Szoecs, and H. Wagner. 2018. vegan: Community Ecology Package. R package version 2.5-2. URL: CRAN.R-project.org/package=vegan.
Quispe-Melgar, H. R., C. S. Sevillano-Ríos, W. C. Navarro Romo, F. N. Ames-Martínez, V. Camel, J. Fjeldså, and M. Kessler. 2019. The Central Andes of Peru: a key area for the conservation of Polylepis forest biodiversity. Journal of Ornithology 161:217-228. https://doi.org/10.1007/s10336-019-01703-5.
Ralph, C. J., G. R. Geupel, P. Pyle, T. E. Martin, and D. F. DeSante. 1993. Handbook of field methods for monitoring landbirds. USDA Forest Service. General Technical Report PSW-GTR-144. Pacific Southwest Research Station, Albany, California, USA. https://doi.org/10.2737/PSW-GTR-144.
Ramsay, P. M. 1992. The Paramo Vegetation of Ecuador: the Community Ecology, Dynamics and Productivity of Tropical Grasslands in the Andes. Doctoral dissertation. University of Wales. U. C. N. W., Bangor: Biological Sciences.
Remsen, J. V. Jr., J. I. Areta, E. Bonaccorso, S. Claramunt, A. Jaramillo, J. F. Pacheco, C. Ribas, M. B. Robbins, F. G. Stiles, D. F. Stotz, and K. J. Zimmer. Version 9 October 2019. A classification of the bird species of South America. (American Ornithological Society). URL: tinyurl.com/yye434xe.
Rodríguez - Girón, S., F. Rodas, A. Schubert, and S. Vasco Tapia. 2014. Área de Biosfera Macizo del Cajas, Experiencias de Desarrollo Sostenible para el Buen Vivir (Cajas Massif Biosphere Area-Sustainable Development Experiences for Good Living). ETAPA EP, Municipio de Cuenca, Ministerio del Ambiente, SENPLADES, Ministerio de Relaciones Exteriores, Cooperación Alemana GIZ, Naturaleza y Cultura Internacional. Cuenca, Ecuador.
Sala, O. E., F. S. Chapin, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-Sanwald, F. L. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker, and D. H. Wall. 2000. Global biodiversity scenarios for the year 2100. Science 287:1770-1774. https://doi.org/10.1126/science.287.5459.1770.
Sarmiento, F. O. 2000. Breaking Mountain Paradigms: Ecological Effects on Human Impacts in Man-aged tropandean Landscapes. AMBIO: A J Hum Environ 29:423-432. https://doi.org/10.1579/0044-7447-29.7.423.
Sierra, R. 1999. Propuesta Preliminar de un Sistema De Clasificación De Vegetación para el Ecuador Continental. Proyecto INEFAN/GEF-BIRF. EcoCiencia: Quito, Ecuador.
Stattersfield, A. J., M. J. Crosby, A. J. Long, and D. C. Wege. 1998. Endemic bird areas of the world. Priorities for biodiversity conservation. Cambridge, UK: BirdLife International, Conservation Series 7.
Stotz, D. F., J. W. Fitzpatrick, T. A. Parker III, and D. K. Moskovits. 1996. Neotropical birds: ecology and conservation. University of Chicago Press. Chicago (USA).
Suárez, E., and G. Medina. 2001. Vegetation structure and soil properties in Ecuadorian Páramo Grasslands with different histories of burning and grazing. Arctic, Antarctic, and Alpine Research 33:158-164. https://doi.org/10.2307/1552216.
Sylvester, S. P., F. Heitkamp, M. D. Sylvester, H. F. Jungkunst, H. J. Sipman, J. M. Toivonen, C. A. Gonzales Inca, J. C. Ospina, and M. Kessler. 2017. Relict high-Andean ecosystems challenge our concepts of naturalness and human impact. Scientific reports 7:1-13. https://doi.org/10.1038/s41598-017-03500-7.
Tews, J., U. Brose, V. Grimm, K. Tielbörger, M. C. Wichmann, M. Schwager, and F. Jeltsch. 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31:79-92. https://doi.org/10.1046/j.0305- 0270.2003.00994.x.
Tinoco, B. A., P. X. Astudillo, S. C. Latta, and C. H. Graham. 2009. Distribution, Ecology and Conservation of an Endangered Andean Hummingbird: The Violet-throated Metaltail (Metallura Baroni). Bird Conservation International 19(1):63-76. https://doi.org/10.1017/S0959270908007703.
Tinoco, B. A., L. Graham, P. X. Astudillo, A. Nieto, J. M. Aguilar, S. C. Latta, and C. H. Graham. 2019. Survival estimates of bird species across altered habitats in the tropical Andes. J Field Ornithology 90:105-116. https://doi.org/10.1111/jofo.12293.
Verboom, J., R. Foppen, P. Chardon, P. Opdam, and P. Luttikhuizen. 2001. Introducing the key patch approach for habitat networks with persistent populations: an example for marshland birds. Biological Conservation 100:89-101. https://doi.org/10.1016/S0006-3207(00)00210-X.
Young, K. R. 1997. Wildlife conservation in the cultural landscapes of the central Andes. Landscape and Urban Planning 38:137-147. https://doi.org/10.1016/S0169-2046(97)00029-7.
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