A SOCIO-ECOLOGICAL FRAMEWORK FOR MONITORING BIODIVERSITY AND THREAT: A CASE STUDY IN THE OSA AND GOLFITO REGION OF COSTA RICA.
Overview – (1) A literature review of the theoretical foundation and science, focusing on (a) cross taxa biodiversity dynamics and frameworks, (b) linkages between forest structure and composition with biodiversity, and (c) use of UAVs and high-spatial and temporal satellite imagery for monitoring of such. (2) An overview of the study area and the issues present there. (3) An overview of the components and how they fit together to incorporate and address (1) and (2).
Component 1 - A multi-taxa multi-method framework for monitoring biodiversity.
This will develop the theoretical basis for the framework and predicted relationships among approaches, taxa and how they could be integrated. This will be based heavily on literature review and meta-analysis.
Component 2 – A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time.
This component will conduct detailed ecological data collection for multiple taxa within a plot network to assess dynamics and relationships among taxa using a within plot analytical approach, using portions of the framework developed in component 1. Sampling methods will install permanent forest plots using standard measurements, including DBH and species identification. Biodiversity measurements will include audio recorders (2D and 3D layout) for bat and birds, camera traps for mammals, pitfall traps for insects - focusing on beetles, and fruit traps for butterflies. These will be co-located with climate sensors, and plots will be geolocated to enable later integration with remote sensing data. Plots for this study will be located at the Lapa Rios Ecolodge and Osa Verde Ecofarm. Data collection will be conducted from May 2018-August 2019 (and potentially onwards).
Component 3 - A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time and space.
Using plots distributed across the Osa Peninsula and Golfito region, incorporating ones previously established by other researchers (including Robin Chazdon and Betsy Yaap), will conduct a spatial temporal study comparing similarities and differences among plot biodiversity. Building off component 2 and now incorporating additional parts of component 1.
Component 4 - A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time and space integrating field and drone-borne LiDAR and hyperspectral data.
Now including detailed forest structural and composition, and land use and cover, information for the areas surrounding each plot using the GatorEye Unpiloted Flying Laboratory, to understand and model local scale (< 300 meters radius) drivers of biodiversity spatio-temporal dynamics.
Component 5 - A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time and space integrating field, drone-borne LiDAR and hyperspectral data, and dense time stacks of high-resolution satellite imagery.
Use dense temporal stacks of high resolution Planet Lab imagery, combined with ongoing INOGO Mapas efforts, to incorporate landscape scale geospatial analyses, e.g., connectivity and fragmentation, into understanding and biodiversity dynamics (both within and among taxa and across all plots). This portion will scale up from site and local GatorEye drone data to remote sensing satellite data for landscape data analysis.
Component 6 - A multi-taxa multi-method framework for monitoring biodiversity: understanding and integrating the spatio-temporal socio-economic drivers of threats.
This component will work to understand the socio-economic and cultural context of biodiversity dynamics using spatial explicit household questionnaires and participatory mapping in communities across the peninsula, in areas potentially impacting our plots. Collaborations with communities collaborating with the Caminos de Osa project will be incorporated as is feasible. Key topics will include threats, e.g., defaunation from hunting, legal and illegal selective logging and mining, habitat degradation and conversion, etc…
Equipment
Broadbent and Almeyda Zambrano have obtained for this project: (a) 3 SM3 audio recorders with GPS time-synchronization to allow for 3D soundscapes of birds, frogs, and insects. (b) 1 SM4 bat recorder. (c) 5 camera traps. And all required misc items including SD memory cards and rechargeable batteries. (d) 1 arbimon recorder. (e) 1 GPS enabled iPad with bat detector. (d) 3 HOBO climate sensors.
General design of a biodiversity kiosk is to have the bat detector at a center stake with a camera trap and a climate sensor, and the SM3 recorders equally spaced and distance from this stake surrounding the stake at approximately 15 m distance and facing inwards. The circle surrounding the stake would undergo standard forest inventory and mapping to create a permanent plot. Additional biodiversity measurements to occur within the plot at a reduced time step are diversity and abundance of: (1) Nymphalid butterflies using rotting fruit traps, (2) pitfall traps - with a focus on dung beetles, and (3) euclidean bee diversity and abundance.
Plots will be located in an area undergoing drone-based 3D mapping to enable detailed temporal and spatial models of biodiversity dynamics and distribution. 3D models are being created at the largest scale using Pix4D analysis of drone RGB imagery, and at smaller scales using drone LiDAR.
Personnel
Components of this project build off of past, ongoing and future collaborations with: (a) Lapa Rios Ecolodoge, including Guillermo Mulder, (b) Osa Conservation, including Andy Whitworth and Rachel Eplee, (c) SPEC Lab faculty Dr. Almeyda Zambrano and Dr. Broadbent, and (d) undergraduate, including Clare Ols and Sandra Almeyda Zambrano, and graduate students, including Kelsi Davis, and numerous collaborators in Costa Rica and elsewhere, and faculty at Stanford University. SPEC Lab graduate student Beatriz Lopez Gutierrez serves as a research assistant on portions of this project through funding from Dr. Broadbent.
Funding
Additional funding sources are being investigated to support full implementation of this project, specifically components 3+.
Inspiration
Relevant references (sample)
Aide, T. M., Corrada-Bravo, C., Campos-Cerqueira, M., Milan, C., Vega, G., & Alvarez, R. 2013. Real-time bioacoustics monitoring and automated species identification. PeerJ 1: e103.
Altrichter, M., Carrillo, E., Sáenz, J., & K Fuller, T. 2001. White-lipped peccary (Tayassu pecari, Artiodactyla: Tayassuidae) diet and fruit availability in a Costa Rican rain forest. Revista de Biología Tropical, 49(3-4): 1183-1192.
Asner, G. P., Knapp, D. E., Martin, R. E., Tupayachi, R. et al. 2014. Targeted carbon conservation at national scales with high-resolution monitoring. Proceedings of the National Academy of Sciences 111(47): E5016-E5022.
Barbosa, J.M., Broadbent, E.N., and Bitencourt, M.D. 2014. Aboveground biomass estimation by remote sensing: a review of the implications for forest regrowth studies in tropical forests. International Journal of Forestry Research 715796: 1-14.
Barlow, J., Gardner, T.A., Araujo, I.S., Avila-Pires, T.C. et al. 2007. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences 104: 18555-18560.
Barton, D. N., Faith, D. P., Rusch, G. M., Acevedo, H., Paniagua, L., & Castro, M. 2009. Environmental service payments: Evaluating biodiversity conservation trade-offs and cost-efficiency in the Osa Conservation Area, Costa Rica. Journal of environmental management, 90(2): 901-911.
Barrantes, G., Q. Jimenez, J. Lobo, T. Maldonado, M. Quesada, and R. Quesada. 1999. Manejo Forestal y Realidad Nacional en la Peninsula de Osa. San José, Costa Rica: INBio.
Broadbent, E. N., Zambrano, A. M. A., Dirzo, R., Durham, W. H., Driscoll, L., Gallagher, P., ... & Randolph, S. G. 2012. The effect of land use change and ecotourism on biodiversity: a case study of Manuel Antonio, Costa Rica, from 1985 to 2008. Landscape ecology, 27(5), 731-744.
Bustamante, M.C., Roitman, I., Aide, T., Alencar, A., Anderson, L., Aragão, L.E, et al. 2016. Towards an integrated monitoring framework to assess the effects of tropical forest degradation and recovery on carbon stocks and biodiversity. Global Change Biology 22: 92-109.
Caughlin, T. T., Rifai, S. W., Graves, S. J., Asner, G. P. and Bohlman, S. A. 2016. Integrating LiDAR-derived tree height and Landsat satellite reflectance to estimate forest regrowth in a tropical agricultural landscape. Remote Sensing in Ecology and Conservation 2: 190-203.
Chazdon, R. L., Peres, C. A., Dent, D., Sheil, D., Lugo, A. E., Lamb, D., ... & Miller, S. E. 2009. The potential for species conservation in tropical secondary forests. Conservation Biology, 23(6), 1406-1417.
Climate Action and UNEP Report. (2016). [Accessed on March 2016: http://www.climateactionprogramme.org/]
Davies, A. B., and Asner, G. P. 2014. Advances in animal ecology from 3D-LiDAR ecosystem mapping. Trends in ecology & evolution, 29(12), 681-691.
DeVries, P.J., Alexander, L.G., Chacon, I.A. & Fordyce, J.A. 2012. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. Journal of Animal Ecology 81: 472–482.
Galetti, M. and Dirzo, R. 2013. Ecological and evolutionary consequences of living in a defaunated world. Biological Conservation 163: 1-6.
Gardner, T. A., Burgess, N. D., Aguilar-Amuchastegui, N., Barlow, J., Berenguer, E., Clements, T., ... and Khan, S. M. (2012). A framework for integrating biodiversity concerns into national REDD+ programmes. Biological Conservation, 154, 61-71.
Getzin, S., Wiegand, K., and Schöning, I. 2012. Assessing biodiversity in forests using very high resolution images and unmanned aerial vehicles. Methods in Ecology and Evolution 3: 397-404.
Harrison, M. E., Boonman, A., Cheyne, S. M., Husson, S. J., Marchant, N. C., & Struebig, M. J. (2012). Biodiversity monitoring protocols for REDD+: can a one-size-fits-all approach really work?. Tropical Conservation Science, 5(1), 1-11.
Henderson, C. 2002. Birds of Costa Rica: A Field Guide. University of Texas Press, USA.
Krause, B., and Farina, A. 2016. Using ecoacoustic methods to survey the impacts of climate change on biodiversity. Biological Conservation 195: 245-254.
Larsen, T.H. 2016. Core Standardized Methods for Rapid Biological Field Assessment. Conservation International, Arlington, VA.
Martínez-Ramos, M., Ortiz-Rodríguez, I. A., Piñero, D., Dirzo, R., and Sarukhán, J. (2016). Anthropogenic disturbances jeopardize biodiversity conservation within tropical rainforest reserves. Proceedings of the National Academy of Sciences 113(19): 5323-5328.
Miller B. W. 2001. A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring. Acta Chiropterologica 3:93–105.
Morales-Salazar, M.S., Vílchez-Alvarado, B., Chazdon, R.L., Ortiz-Malavasi, E., and Guevara-Bonilla, M. 2013. Estructura, composición y diversidad vegetal en bosques tropicales del Corredor Biológico Osa, Costa Rica. Revista Forestal Mesoamericana Kurú 10(24): 2215-2504.
Moura, N. G., Lees, A. C., Andretti, C. B., Davis, B. J., Solar, R. R., Aleixo, A., ... and Gardner, T. A. 2013. Avian biodiversity in multiple-use landscapes of the Brazilian Amazon. Biological Conservation, 167: 339-348.
Naimi, B., and Araújo, M. B. 2016. sdm: a reproducible and extensible R platform for species distribution modelling. Ecography 39: 1-8.
O'Brien T. G., Baillie J. E. M., Krueger L. and Cuke M. 2010. The Wildlife Picture Index: monitoring top trophic levels. Animal Conservation 13:335–343. Google Scholar.
Osa Conservation. 2017. http://osaconservation.org/. [[Accessed on Abril 2017: http://osaconservation.org/projects/habitat/forest-restoration/ ]
Pekin, B.K., Jung, J., Villanueva-Rivera, L.J., Pijanowski, B.C and Ahumada, J.A. 2012. Modeling acoustic diversity using soundscape recordings and LIDAR-derived metrics of vertical forest structure in a neotropical rainforest. Landscape Ecology 27:1513-1522.
Polidoro, B. A., Dahlquist, R. M., Castillo, L. E., Morra, M. J., Somarriba, E., and Bosque-Pérez, N. A. 2008. Pesticide application practices, pest knowledge, and cost-benefits of plantain production in the Bribri-Cabécar Indigenous Territories, Costa Rica. Environmental Research 108 (1): 98-106.
Poorter, L., Bongers, F., Aide, M.T., Almeyda Zambrano, A.M. et al. 2016. Biomass resilience of Neotropical secondary forests. Nature 530: 211-214.
Martínez-Ramos, M., Ortiz-Rodríguez, I. A., Piñero, D., Dirzo, R., & Sarukhán, J. 2016. Anthropogenic disturbances jeopardize biodiversity conservation within tropical rainforest reserves. Proceedings of the National Academy of Sciences, 113(19): 5323-5328.
Sanchez-Azofeifa, G.A., Daily, G.C., Pfaff, A.S.P., and Busch, C. 2003. Integrity and isolation of Costa Rica’s national parks and biological reserves: Examining the dynamics of land-cover change. Biological Conservation 109(1): 123-135.
Sanchez-Azofeifa, G.A., Rivard, B., Calvo, J., and Moorthy, I. 2002. Dynamics of Tropical Deforestation Around National Parks: Remote Sensing of Forest Change on the Osa Peninsula of Costa Rica. Mountain Research and Development 22(4): 352-358.
Sanchez-Azofeifa, G.A., Bawa, K.S., Quesada-Mateo, C.A., Gonzales-Quesada, P., and Dayanadan, S. 1999. Protected areas and conservation of biodiversity in the tropics. Conservation Biology 13(2): 407-411.
Soto M. 2013. Solo el 4% de las aguas residuales generadas en Costa Rica es tratado antes de ir a los ríos. La Nación, San José (CR). [Accessed on January 2017: http://www.nacion.com/vivir/ambiente/Solo-aguas-residuales-tratado-rios_0_1379462044.html]
SINAC and INBio.2013. IV Informe de país al Convenio sobre la Biodiversidad Biológica. [Accessed on January 2017: http://www.sinac.go.cr/EN-US/docu/Pages/default.aspx]
Smith, P., House, J. I., Bustamante, M., Sobocká, J., Harper, R., Pan, G., ... and Paustian, K. 2016. Global change pressures on soils from land use and management. Global change biology, 22(3): 1008-1028.
Taylor, P., Asner, G., Dahlin, K., Anderson, C. et al. 2015. Landscape-scale controls on aboveground forest carbon stocks on the Osa Peninsula, Costa Rica. PloS one 10(6): e0126748.
Thomas, L., Buckland, S.T., Rexstad, E.A., Laake, J.L., Strindberg, S., Hedley, S.L., Bishop, J.R.B., Marques, T.A. & Burnham, K.P. (2010). Distance software: design and analysis sampling surveys for estimating population size. Journal of Applied Ecology 47: 5-14.
Thompson, I.., Mackey, B., McNulty, S., Mosseler, A. 2009. Forest Resilience, Biodiversity, and Climate Change. A synthesis of the biodiversity/resilience/stability relationship in forest ecosystems. Secretariat of the Convention on Biological Diversity 43: 1-67.
Torres, N. M., De Marco, P., Santos, T., Silveira, L., de Almeida Jácomo, A. T., & Diniz‐Filho, J. A. 2012. Can species distribution modelling provide estimates of population densities? A case study with jaguars in the Neotropics. Diversity and Distributions 18(6): 615-627
Vílchez Alvarado, B., Chazdon, R., and Milla, V. 2008. Dinámica de la regeneración en cuatro bosques secundarios tropicales de la región Huetar Norte, Costa Rica: Su valor para la conservación o uso comercial. Recursos Naturales y Ambiente 55: 118-128.
Waldon, J., Miller, B. W., & Miller, C. M. .2011.. A model biodiversity monitoring protocol for REDD projects. Tropical Conservation Science, 4(3), 254-260.
Weissenhofer, A., Hastik, R., Jenking, D., and Huber, W. B. 2012. Biological Corridors in the Golfo Dulce region: a project to preserve the region’s biodiversity through conservation, reforestation and restoration. [Accessed on January 2017: https://www.lagamba.at/uploads/media/Nutzholz_corredor_01.pdf]
Wildlife Acoustics. 2017. Bioacoustic Monitoring Systems. [Accessed on March 2017: https://www.wildlifeacoustics.com/]
Zamora‐Gutierrez, V., Lopez‐Gonzalez, C., MacSwiney Gonzalez, M. C., Fenton, B. et al. 2016. Acoustic identification of Mexican bats based on taxonomic and ecological constraints on call design. Methods in Ecology and Evolution 7(9): 1082-1091.
Overview – (1) A literature review of the theoretical foundation and science, focusing on (a) cross taxa biodiversity dynamics and frameworks, (b) linkages between forest structure and composition with biodiversity, and (c) use of UAVs and high-spatial and temporal satellite imagery for monitoring of such. (2) An overview of the study area and the issues present there. (3) An overview of the components and how they fit together to incorporate and address (1) and (2).
Component 1 - A multi-taxa multi-method framework for monitoring biodiversity.
This will develop the theoretical basis for the framework and predicted relationships among approaches, taxa and how they could be integrated. This will be based heavily on literature review and meta-analysis.
Component 2 – A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time.
This component will conduct detailed ecological data collection for multiple taxa within a plot network to assess dynamics and relationships among taxa using a within plot analytical approach, using portions of the framework developed in component 1. Sampling methods will install permanent forest plots using standard measurements, including DBH and species identification. Biodiversity measurements will include audio recorders (2D and 3D layout) for bat and birds, camera traps for mammals, pitfall traps for insects - focusing on beetles, and fruit traps for butterflies. These will be co-located with climate sensors, and plots will be geolocated to enable later integration with remote sensing data. Plots for this study will be located at the Lapa Rios Ecolodge and Osa Verde Ecofarm. Data collection will be conducted from May 2018-August 2019 (and potentially onwards).
Component 3 - A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time and space.
Using plots distributed across the Osa Peninsula and Golfito region, incorporating ones previously established by other researchers (including Robin Chazdon and Betsy Yaap), will conduct a spatial temporal study comparing similarities and differences among plot biodiversity. Building off component 2 and now incorporating additional parts of component 1.
Component 4 - A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time and space integrating field and drone-borne LiDAR and hyperspectral data.
Now including detailed forest structural and composition, and land use and cover, information for the areas surrounding each plot using the GatorEye Unpiloted Flying Laboratory, to understand and model local scale (< 300 meters radius) drivers of biodiversity spatio-temporal dynamics.
Component 5 - A multi-taxa multi-method framework for monitoring biodiversity: correlations among taxa across time and space integrating field, drone-borne LiDAR and hyperspectral data, and dense time stacks of high-resolution satellite imagery.
Use dense temporal stacks of high resolution Planet Lab imagery, combined with ongoing INOGO Mapas efforts, to incorporate landscape scale geospatial analyses, e.g., connectivity and fragmentation, into understanding and biodiversity dynamics (both within and among taxa and across all plots). This portion will scale up from site and local GatorEye drone data to remote sensing satellite data for landscape data analysis.
Component 6 - A multi-taxa multi-method framework for monitoring biodiversity: understanding and integrating the spatio-temporal socio-economic drivers of threats.
This component will work to understand the socio-economic and cultural context of biodiversity dynamics using spatial explicit household questionnaires and participatory mapping in communities across the peninsula, in areas potentially impacting our plots. Collaborations with communities collaborating with the Caminos de Osa project will be incorporated as is feasible. Key topics will include threats, e.g., defaunation from hunting, legal and illegal selective logging and mining, habitat degradation and conversion, etc…
Equipment
Broadbent and Almeyda Zambrano have obtained for this project: (a) 3 SM3 audio recorders with GPS time-synchronization to allow for 3D soundscapes of birds, frogs, and insects. (b) 1 SM4 bat recorder. (c) 5 camera traps. And all required misc items including SD memory cards and rechargeable batteries. (d) 1 arbimon recorder. (e) 1 GPS enabled iPad with bat detector. (d) 3 HOBO climate sensors.
General design of a biodiversity kiosk is to have the bat detector at a center stake with a camera trap and a climate sensor, and the SM3 recorders equally spaced and distance from this stake surrounding the stake at approximately 15 m distance and facing inwards. The circle surrounding the stake would undergo standard forest inventory and mapping to create a permanent plot. Additional biodiversity measurements to occur within the plot at a reduced time step are diversity and abundance of: (1) Nymphalid butterflies using rotting fruit traps, (2) pitfall traps - with a focus on dung beetles, and (3) euclidean bee diversity and abundance.
Plots will be located in an area undergoing drone-based 3D mapping to enable detailed temporal and spatial models of biodiversity dynamics and distribution. 3D models are being created at the largest scale using Pix4D analysis of drone RGB imagery, and at smaller scales using drone LiDAR.
Personnel
Components of this project build off of past, ongoing and future collaborations with: (a) Lapa Rios Ecolodoge, including Guillermo Mulder, (b) Osa Conservation, including Andy Whitworth and Rachel Eplee, (c) SPEC Lab faculty Dr. Almeyda Zambrano and Dr. Broadbent, and (d) undergraduate, including Clare Ols and Sandra Almeyda Zambrano, and graduate students, including Kelsi Davis, and numerous collaborators in Costa Rica and elsewhere, and faculty at Stanford University. SPEC Lab graduate student Beatriz Lopez Gutierrez serves as a research assistant on portions of this project through funding from Dr. Broadbent.
Funding
Additional funding sources are being investigated to support full implementation of this project, specifically components 3+.
Inspiration
Relevant references (sample)
Aide, T. M., Corrada-Bravo, C., Campos-Cerqueira, M., Milan, C., Vega, G., & Alvarez, R. 2013. Real-time bioacoustics monitoring and automated species identification. PeerJ 1: e103.
Altrichter, M., Carrillo, E., Sáenz, J., & K Fuller, T. 2001. White-lipped peccary (Tayassu pecari, Artiodactyla: Tayassuidae) diet and fruit availability in a Costa Rican rain forest. Revista de Biología Tropical, 49(3-4): 1183-1192.
Asner, G. P., Knapp, D. E., Martin, R. E., Tupayachi, R. et al. 2014. Targeted carbon conservation at national scales with high-resolution monitoring. Proceedings of the National Academy of Sciences 111(47): E5016-E5022.
Barbosa, J.M., Broadbent, E.N., and Bitencourt, M.D. 2014. Aboveground biomass estimation by remote sensing: a review of the implications for forest regrowth studies in tropical forests. International Journal of Forestry Research 715796: 1-14.
Barlow, J., Gardner, T.A., Araujo, I.S., Avila-Pires, T.C. et al. 2007. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences 104: 18555-18560.
Barton, D. N., Faith, D. P., Rusch, G. M., Acevedo, H., Paniagua, L., & Castro, M. 2009. Environmental service payments: Evaluating biodiversity conservation trade-offs and cost-efficiency in the Osa Conservation Area, Costa Rica. Journal of environmental management, 90(2): 901-911.
Barrantes, G., Q. Jimenez, J. Lobo, T. Maldonado, M. Quesada, and R. Quesada. 1999. Manejo Forestal y Realidad Nacional en la Peninsula de Osa. San José, Costa Rica: INBio.
Broadbent, E. N., Zambrano, A. M. A., Dirzo, R., Durham, W. H., Driscoll, L., Gallagher, P., ... & Randolph, S. G. 2012. The effect of land use change and ecotourism on biodiversity: a case study of Manuel Antonio, Costa Rica, from 1985 to 2008. Landscape ecology, 27(5), 731-744.
Bustamante, M.C., Roitman, I., Aide, T., Alencar, A., Anderson, L., Aragão, L.E, et al. 2016. Towards an integrated monitoring framework to assess the effects of tropical forest degradation and recovery on carbon stocks and biodiversity. Global Change Biology 22: 92-109.
Caughlin, T. T., Rifai, S. W., Graves, S. J., Asner, G. P. and Bohlman, S. A. 2016. Integrating LiDAR-derived tree height and Landsat satellite reflectance to estimate forest regrowth in a tropical agricultural landscape. Remote Sensing in Ecology and Conservation 2: 190-203.
Chazdon, R. L., Peres, C. A., Dent, D., Sheil, D., Lugo, A. E., Lamb, D., ... & Miller, S. E. 2009. The potential for species conservation in tropical secondary forests. Conservation Biology, 23(6), 1406-1417.
Climate Action and UNEP Report. (2016). [Accessed on March 2016: http://www.climateactionprogramme.org/]
Davies, A. B., and Asner, G. P. 2014. Advances in animal ecology from 3D-LiDAR ecosystem mapping. Trends in ecology & evolution, 29(12), 681-691.
DeVries, P.J., Alexander, L.G., Chacon, I.A. & Fordyce, J.A. 2012. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. Journal of Animal Ecology 81: 472–482.
Galetti, M. and Dirzo, R. 2013. Ecological and evolutionary consequences of living in a defaunated world. Biological Conservation 163: 1-6.
Gardner, T. A., Burgess, N. D., Aguilar-Amuchastegui, N., Barlow, J., Berenguer, E., Clements, T., ... and Khan, S. M. (2012). A framework for integrating biodiversity concerns into national REDD+ programmes. Biological Conservation, 154, 61-71.
Getzin, S., Wiegand, K., and Schöning, I. 2012. Assessing biodiversity in forests using very high resolution images and unmanned aerial vehicles. Methods in Ecology and Evolution 3: 397-404.
Harrison, M. E., Boonman, A., Cheyne, S. M., Husson, S. J., Marchant, N. C., & Struebig, M. J. (2012). Biodiversity monitoring protocols for REDD+: can a one-size-fits-all approach really work?. Tropical Conservation Science, 5(1), 1-11.
Henderson, C. 2002. Birds of Costa Rica: A Field Guide. University of Texas Press, USA.
Krause, B., and Farina, A. 2016. Using ecoacoustic methods to survey the impacts of climate change on biodiversity. Biological Conservation 195: 245-254.
Larsen, T.H. 2016. Core Standardized Methods for Rapid Biological Field Assessment. Conservation International, Arlington, VA.
Martínez-Ramos, M., Ortiz-Rodríguez, I. A., Piñero, D., Dirzo, R., and Sarukhán, J. (2016). Anthropogenic disturbances jeopardize biodiversity conservation within tropical rainforest reserves. Proceedings of the National Academy of Sciences 113(19): 5323-5328.
Miller B. W. 2001. A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring. Acta Chiropterologica 3:93–105.
Morales-Salazar, M.S., Vílchez-Alvarado, B., Chazdon, R.L., Ortiz-Malavasi, E., and Guevara-Bonilla, M. 2013. Estructura, composición y diversidad vegetal en bosques tropicales del Corredor Biológico Osa, Costa Rica. Revista Forestal Mesoamericana Kurú 10(24): 2215-2504.
Moura, N. G., Lees, A. C., Andretti, C. B., Davis, B. J., Solar, R. R., Aleixo, A., ... and Gardner, T. A. 2013. Avian biodiversity in multiple-use landscapes of the Brazilian Amazon. Biological Conservation, 167: 339-348.
Naimi, B., and Araújo, M. B. 2016. sdm: a reproducible and extensible R platform for species distribution modelling. Ecography 39: 1-8.
O'Brien T. G., Baillie J. E. M., Krueger L. and Cuke M. 2010. The Wildlife Picture Index: monitoring top trophic levels. Animal Conservation 13:335–343. Google Scholar.
Osa Conservation. 2017. http://osaconservation.org/. [[Accessed on Abril 2017: http://osaconservation.org/projects/habitat/forest-restoration/ ]
Pekin, B.K., Jung, J., Villanueva-Rivera, L.J., Pijanowski, B.C and Ahumada, J.A. 2012. Modeling acoustic diversity using soundscape recordings and LIDAR-derived metrics of vertical forest structure in a neotropical rainforest. Landscape Ecology 27:1513-1522.
Polidoro, B. A., Dahlquist, R. M., Castillo, L. E., Morra, M. J., Somarriba, E., and Bosque-Pérez, N. A. 2008. Pesticide application practices, pest knowledge, and cost-benefits of plantain production in the Bribri-Cabécar Indigenous Territories, Costa Rica. Environmental Research 108 (1): 98-106.
Poorter, L., Bongers, F., Aide, M.T., Almeyda Zambrano, A.M. et al. 2016. Biomass resilience of Neotropical secondary forests. Nature 530: 211-214.
Martínez-Ramos, M., Ortiz-Rodríguez, I. A., Piñero, D., Dirzo, R., & Sarukhán, J. 2016. Anthropogenic disturbances jeopardize biodiversity conservation within tropical rainforest reserves. Proceedings of the National Academy of Sciences, 113(19): 5323-5328.
Sanchez-Azofeifa, G.A., Daily, G.C., Pfaff, A.S.P., and Busch, C. 2003. Integrity and isolation of Costa Rica’s national parks and biological reserves: Examining the dynamics of land-cover change. Biological Conservation 109(1): 123-135.
Sanchez-Azofeifa, G.A., Rivard, B., Calvo, J., and Moorthy, I. 2002. Dynamics of Tropical Deforestation Around National Parks: Remote Sensing of Forest Change on the Osa Peninsula of Costa Rica. Mountain Research and Development 22(4): 352-358.
Sanchez-Azofeifa, G.A., Bawa, K.S., Quesada-Mateo, C.A., Gonzales-Quesada, P., and Dayanadan, S. 1999. Protected areas and conservation of biodiversity in the tropics. Conservation Biology 13(2): 407-411.
Soto M. 2013. Solo el 4% de las aguas residuales generadas en Costa Rica es tratado antes de ir a los ríos. La Nación, San José (CR). [Accessed on January 2017: http://www.nacion.com/vivir/ambiente/Solo-aguas-residuales-tratado-rios_0_1379462044.html]
SINAC and INBio.2013. IV Informe de país al Convenio sobre la Biodiversidad Biológica. [Accessed on January 2017: http://www.sinac.go.cr/EN-US/docu/Pages/default.aspx]
Smith, P., House, J. I., Bustamante, M., Sobocká, J., Harper, R., Pan, G., ... and Paustian, K. 2016. Global change pressures on soils from land use and management. Global change biology, 22(3): 1008-1028.
Taylor, P., Asner, G., Dahlin, K., Anderson, C. et al. 2015. Landscape-scale controls on aboveground forest carbon stocks on the Osa Peninsula, Costa Rica. PloS one 10(6): e0126748.
Thomas, L., Buckland, S.T., Rexstad, E.A., Laake, J.L., Strindberg, S., Hedley, S.L., Bishop, J.R.B., Marques, T.A. & Burnham, K.P. (2010). Distance software: design and analysis sampling surveys for estimating population size. Journal of Applied Ecology 47: 5-14.
Thompson, I.., Mackey, B., McNulty, S., Mosseler, A. 2009. Forest Resilience, Biodiversity, and Climate Change. A synthesis of the biodiversity/resilience/stability relationship in forest ecosystems. Secretariat of the Convention on Biological Diversity 43: 1-67.
Torres, N. M., De Marco, P., Santos, T., Silveira, L., de Almeida Jácomo, A. T., & Diniz‐Filho, J. A. 2012. Can species distribution modelling provide estimates of population densities? A case study with jaguars in the Neotropics. Diversity and Distributions 18(6): 615-627
Vílchez Alvarado, B., Chazdon, R., and Milla, V. 2008. Dinámica de la regeneración en cuatro bosques secundarios tropicales de la región Huetar Norte, Costa Rica: Su valor para la conservación o uso comercial. Recursos Naturales y Ambiente 55: 118-128.
Waldon, J., Miller, B. W., & Miller, C. M. .2011.. A model biodiversity monitoring protocol for REDD projects. Tropical Conservation Science, 4(3), 254-260.
Weissenhofer, A., Hastik, R., Jenking, D., and Huber, W. B. 2012. Biological Corridors in the Golfo Dulce region: a project to preserve the region’s biodiversity through conservation, reforestation and restoration. [Accessed on January 2017: https://www.lagamba.at/uploads/media/Nutzholz_corredor_01.pdf]
Wildlife Acoustics. 2017. Bioacoustic Monitoring Systems. [Accessed on March 2017: https://www.wildlifeacoustics.com/]
Zamora‐Gutierrez, V., Lopez‐Gonzalez, C., MacSwiney Gonzalez, M. C., Fenton, B. et al. 2016. Acoustic identification of Mexican bats based on taxonomic and ecological constraints on call design. Methods in Ecology and Evolution 7(9): 1082-1091.
