Diversity of indicator groups in the analysis of environmental compensation: Its application in the case of the Río Piedras Reservoir, Costa Rica

Authors

  • Mahmood Sasa Escuela de Biología y Centro de Investigaciones en Biodiversidad y Ecología Tropical, Universidad de Costa Rica, San José, Costa Rica. Instituto Clodomiro Picado, Universidad de Costa Rica, San José, Costa Rica. Author https://orcid.org/0000-0003-0118-5142
  • Federico Oviedo-Brenes Estación Biológica Palo Verde, Organización para Estudios Tropicales, Guanacaste, Costa Rica Author
  • Davinia Beneyto-Garrigos Escuela de Biología y Centro de Investigaciones en Biodiversidad y Ecología Tropical, Universidad de Costa Rica, San José, Costa Rica. Estación Biológica Palo Verde, Organización para Estudios Tropicales, Guanacaste, Costa Rica. Author https://orcid.org/0000-0003-0609-9905
  • Fabián Bonilla Instituto Clodomiro Picado, Universidad de Costa Rica, San José, Costa Rica Author https://orcid.org/0000-0002-5095-2750
  • J.-Edgardo Arevalo Escuela de Biología y Centro de Investigaciones en Biodiversidad y Ecología Tropical, Universidad de Costa Rica, San José, Costa Rica. The School for Field Studies, Atenas, Costa Rica. Author https://orcid.org/0000-0003-4160-8373
  • Ragde Sánchez Asociación Theria Author
  • Lilliam Morales-Gutiérrez Estación Biológica Palo Verde, Organización para Estudios Tropicales, Guanacaste, Costa Rica Author https://orcid.org/0000-0002-6599-9076
  • Jazmín Arias-Ortega Instituto Clodomiro Picado, Universidad de Costa Rica, San José, Costa Rica Author https://orcid.org/0000-0002-6983-4252
  • Ronald Vargas-Castro Soltis Center for Research & Education. University Texas A & M University. Author
  • Juan Serrano-Sandí Estación Biológica Palo Verde, Organización para Estudios Tropicales, Guanacaste, Costa Rica Author https://orcid.org/0000-0003-1780-3064
  • Juan-S. Monrós Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universidad de Valencia, Valencia, España Author https://orcid.org/0000-0002-0952-2089
  • Paul Hanson Escuela de Biología y Centro de Investigaciones en Biodiversidad y Ecología Tropical, Universidad de Costa Rica, San José, Costa Rica Author https://orcid.org/0000-0002-7667-7718

DOI:

https://doi.org/10.15517/rev.biol.trop..v70iS1.53487

Keywords:

Bioindicators, environmental offsets, biodiversity, impact study, ecological equivalence, species wealth.

Abstract

Introducción: Cerca de 113 hectáreas dentro de la Reserva Biológica Lomas de Barbudal (RBLB) se inundarían si se llegara a establecer el embalse de riego Río Piedras en el noroeste de Costa Rica. Ante ese impacto inevitable, la legislación costarricense requiere evaluar la pérdida de diversidad en el sitio y compensarla siguiendo el principio de equivalencia ecológica.

Objetivo: Nuestro objetivo fue evaluar la pérdida de diversidad en el sitio y, valorar esta condición en una propiedad privada adyacente considerada como sitio potencial para compensar por esas pérdidas.

Metodología: La diversidad, composición y prioridad de conservación de plantas vasculares, fauna vertebrada y artrópodos del sotobosque fueron evaluadas en el sitio de inundación en RBLB y en una propiedad privada adyacente identificada como sitio potencial de compensación. La equivalencia en diversidad entre ambos sitios se valoró mediante un procedimiento que asigna puntajes a los diferentes indicadores del sitio de compensación respecto a los observados en RBLB. La suma de esos puntajes representa la condición de diversidad del sitio de compensación y puede utilizarse como criterio para fundamentar acciones resarcitorias.  

Resultados: Todos los grupos sustitutos registraron un alto número de especies, aunque la información aportada por las plantas herbáceas, los mamíferos no voladores y los reptiles fue limitada. En contraste, los otros grupos indican una mayor diversidad en el sitio potencial de inundación, atribuida a sutiles diferencias ambientales y a su mejor conservación. En consecuencia, se valoró sustituir el área afectada por un área mayor del sitio de compensación para resarcir las perdidas en diversidad estimadas.

Conclusión: Nuestro análisis muestra que grupos sustitutos pueden ser empleados en estudios ambientales a corto plazo. Sin embargo, los grupos a utilizar deben seleccionarse cuidadosamente, considerando los objetivos y el alcance del proyecto. Cuantificar la condición de diversidad del sitio de compensación respecto a la que se encuentra en un sitio de referencia parece ser un procedimiento válido, repetible y evaluable que permite establecer criterios sobre los cuales basar medidas resarcitorias.

Downloads

Download data is not yet available.

References

Alho, C. J. R. (2011). Environmental effects of hydropower reservoirs on wild mammals and freshwater turtles in Amazonia: a review. Oecologia Australis, 15, 593–604. DOI: https://doi.org/10.4257/oeco.2011.1503.11

Anand, M., Laurence, S., & Rayfield, B. (2005). Diversity relationships among taxonomic groups in recovering and restored forests. Conservation Biology, 19, 955–962. DOI: https://doi.org/10.1111/j.1523-1739.2005.00571.x

Andersen, A. N. (1997). Using ants as bioindicators: multiscale issues in ant community ecology. Conservation Ecology, 1(1), 1–10. DOI: https://doi.org/10.5751/ES-00014-010108

Andersen, A. N., & Müller, W. J. (2000). Arthropod responses to experimental fire regimes in an Australian tropical savannah: ordinal‐level analysis. Austral Ecology, 25(2), 199–209. DOI: https://doi.org/10.1046/j.1442-9993.2000.01038.x

Arthington, A. H., & McKenzie, F. (1997). Review of impacts of displaced/introduced fauna associated with inland waters. Canberra: Environment Australia.

Azeria, E. T., Fortin, D., Hébert, C., Peres-Neto, P., Pothier, D., & Ruel, J. C. (2009). Using null model analysis of species co-occurrences to deconstruct biodiversity patterns and select indicator species. Diversity and Distributions, 15(6), 958–971. DOI: https://doi.org/10.1111/j.1472-4642.2009.00613.x

Báldi, A. (2003). Using higher taxa as surrogates of species richness: a study based on 3700 Coleoptera, Diptera, and Acari species in Central-Hungarian reserves. Basic and applied Ecology, 4(6), 589–593. DOI: https://doi.org/10.1078/1439-1791-00193

Balestra, V., Celli, G., & Porrini, C. (1992). Bees, honey, larvae and pollen in biomonitoring of atmospheric pollution. Aerobiologia, 8(1), 122–126. DOI: https://doi.org/10.1007/BF02291339

Barua, M. (2011). Mobilizing metaphors: the popular use of keystone, flagship and umbrella species concepts. Biodiversity and Conservation, 20(7), 1427–1440. DOI: https://doi.org/10.1007/s10531-011-0035-y

Beck, B. B., Rapaport, L. G., Price, M. R., & Wilson, A. C. (1994). Reintroduction of captive-born animals. . In P.J.S. Olney, G.M. Mace, A.T.C. Feistner, (Eds.), Creative conservation (pp. 265–286). Springer, Dordrecht. DOI: https://doi.org/10.1007/978-94-011-0721-1_13

Benayas, J. M. R., Newton, A. C., Diaz, A., & Bullock, J. M. (2009). Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science, 325(5944), 1121–1124. DOI: https://doi.org/10.1126/science.1172460

Blair, R. B. (1999). Birds and butterflies along an urban gradient: surrogate taxa for assessing biodiversity? Ecological applications, 9(1), 164–170. DOI: https://doi.org/10.1890/1051-0761(1999)009[0164:BABAAU]2.0.CO;2

Bonilla, F., Oviedo-Brenes, F., Beneyto-Garrigos, D., Arevalo, E., Morales-Gutiérrez, L., Serrano-Sandí, J., & Sasa, M. (2022). Aplicación del método de Hábitat-Hectárea en compensación ambiental: El caso del Embalse Río Piedras, Costa Rica. Revista de Biología Tropical, 70(S1), e52283. DOI: https://doi.org/10.15517/rev.biol.trop.2022.52283

Büchs, W. (2003). Biodiversity and agri-environmental indicators—general scopes and skills with special reference to the habitat level. Agriculture, Ecosystems & Environment, 98(1–3), 35–78. DOI: https://doi.org/10.1016/S0167-8809(03)00070-7

Bussing, W. A. (1998). Freshwater fishes of Costa Rica (Vol. 46). Editorial Universidad de Costa Rica.

Bussing, W. A., & López, M. I. (1977). Distribución y aspectos ecológicos de los peces de las cuencas hidrográficas de Arenal, Bebedero y Tempisque, Costa Rica. Revista de Biología Tropical, 25(1), 13–37.

Bussing, W. A., & López, M. I. (1996). Fishes collected during the victor Hensen Costa Rica expedition (1993/1994). Revista de Biología Tropical, 44(S3), 183–186.

Butler, D. W. (2009). Planning iterative investment for landscape restoration: Choice of biodiversity indicator makes a difference. Biological Conservation, 142(10), 2202–2216. DOI: https://doi.org/10.1016/j.biocon.2009.04.023

Cajiao, M. V. (2019). Ley 9610 para la modificación de límites de la Reserva Biológica Lomas de Barbudal. Ambientico, 269, 70–73.

Calderón-Patrón, J. M., Moreno, C. E., & Zuria, I. (2012). La diversidad beta: medio siglo de avances. Revista mexicana de biodiversidad, 83(3), 879–891. DOI: https://doi.org/10.22201/ib.20078706e.2012.3.992

Calle, I., Zabarburu, S., & Mora, C. (2014). Compensación Ambiental: Una oportunidad para la adecuada gestión de los impactos ambientales en el Perú. Sociedad Peruana de Derecho Ambiental. https://repositorio.spda.org.pe/bitstream/20.500.12823/142/1/Compensacion_Ambiental_2014.pdf

Chiarucci, A., Bacaro, G., Rocchini, D., & Fattorini, L. (2008). Discovering and rediscovering the sample-based rarefaction formula in the ecological literature. Community Ecology, 9(1), 121–123. DOI: https://doi.org/10.1556/ComEc.9.2008.1.14

Connell, J. H. (1978). Diversity in tropical rain forests and coral reefs: high diversity of trees and corals is maintained only in a nonequilibrium state. Science, 199(4335), 1302–1310. DOI: https://doi.org/10.1126/science.199.4335.1302

Cowell, R. (1997). Stretching the limits: environmental compensation, habitat creation and DOI: https://doi.org/10.1111/j.0020-2754.1997.00292.x

sustainable development. Transactions of the Institute of British Geographers, 22, 292–306.

Crisp, P. N., Dickinson, K. J. M., & Gibbs, G. W. (1998). Does native invertebrate diversity reflect native plant diversity? A case study from New Zealand and implications for conservation. Biological Conservation, 83(2), 209–220. DOI: https://doi.org/10.1016/S0006-3207(97)00053-0

Cuperus, R. (2005). Ecological compensation of highway impacts; negotiated trade-off or no-net-loss? Leiden University.

Díaz-Reyes, C.E. (2014). Enfoques teóricos y metodológicos de las compensaciones ambientales en el contexto de la Evaluación de Impacto Ambiental en Colombia. [Tesis de Maestría, Universidad Nacional de Colombia]. Repositorio institucional de la Universidad Nacional de Colombia. http://repositorio.unal.edu.co/handle/unal/52252

Dickens, M. J., Delehanty, D. J., & Romero, L. M. (2009). Stress and translocation: alterations in the stress physiology of translocated birds. Proceedings of the Royal Society B: Biological Sciences, 276(1664), 2051–2056. DOI: https://doi.org/10.1098/rspb.2008.1778

Failing, L., Gregory, R. (2003). Ten common mistakes in designing biodiversity indicators for forest policy. Journal of Environmental Management, 68, 121–132. DOI: https://doi.org/10.1016/S0301-4797(03)00014-8

Faro, C., Ramalho-Santos, M., Vieira, M., Mendes, A., Simões, I., Andrade, R., Veríssimo, P., Lin, X., Tang, J., & Pires, E. 1999. Cloning and characterization of a cDNA encoding cardosin A, an RGD-containing plant aspartic proteinase. Journal of Biological Chemistry, 274(40), 28724–28729.. DOI: https://doi.org/10.1074/jbc.274.40.28724

Fausch, K. D., Lyons, J. O. H. N., Karr, J. R., & Angermeier, P. L. (1990). Fish communities as indicators of environmental degradation. American fisheries society symposium, 8(1), 123–144.

Forbes, D. (2006). Reintroducción, exitosa, de la lapa roja (Ara macao) en los bosques secos y húmedos de Costa Rica: supervivencia, movimientos y dieta. Mesoamericana, 10(2), 62–68.

García-Morales, R., Moreno, C. E., & Bello-Gutiérrez, J. (2011). Renovando las medidas para evaluar la diversidad en comunidades ecológicas: el número de especies efectivas de murciélagos en el sureste de Tabasco, México. Therya, 2(3), 205–215. DOI: https://doi.org/10.12933/therya-11-47

García Valdés, M., & Suárez Marín, M. (2013). Delphi method for the expert consultation in the scientific research. Revista Cubana de Salud Pública, 39(2), 253–267.

Gart, J. J., Siegel, A. F., & German, R. Z. (1982). Rarefaction and taxonomic diversity. Biometrics, 38(1), 235–241. DOI: https://doi.org/10.2307/2530306

Gaston, K., Gauld, I., & Hanson, P. (1996). The size and composition of the hymenopteran fauna of Costa Rica. Journal of Biogeography, 23(1), 105–113. DOI: https://doi.org/10.1046/j.1365-2699.1996.00978.x

Gerhardt, F. (2003). Abiotic and biotic resistance to plant invasions of vernal pools in the central valley of California, United States. University of Colorado at Boulder. DOI: https://doi.org/10.1046/j.1365-2699.2003.00911.x

Germano, J. M., & Bishop, P. J. (2009). Suitability of amphibians and reptiles for translocation. Conservation Biology, 23(1), 7–15. DOI: https://doi.org/10.1111/j.1523-1739.2008.01123.x

Giehl, N. F. D. S., Cabette, H. S. R., Dias-Silva, K., Juen, L., Moreira, F. F. F., de Castro, L. A., Ferreira, V. R. S., & Batista, J. D. (2020). Variation in the diversity of semiaquatic bugs (Insecta: Heteroptera: Gerromorpha) in altered and preserved veredas. Hydrobiologia, 847(16), 3497-3510. DOI: https://doi.org/10.1007/s10750-020-04364-1

Gillespie, T. W., Grijalva, A., & Farris, C. N. (2000). Diversity, composition, and structure of tropical dry forests in Central America. Plant Ecology, 147(1), 37–47. DOI: https://doi.org/10.1023/A:1009848525399

Gillespie, T. W., & Walter, H. (2001). Distribution of bird species richness at a regional scale in tropical dry forest of Central America. Journal of Biogeography, 28(5), 651–662. DOI: https://doi.org/10.1046/j.1365-2699.2001.00575.x

Godfray, H. C. J., Lewis, O. T., & Memmott, J. (1999). Studying insect diversity in the tropics. Changes and Disturbance in Tropical Rainforest in South-East Asia, 1, 87–100. DOI: https://doi.org/10.1142/9781848160125_0008

Greene, H. W. (2005). Organisms in nature as a central focus for biology. Trends in Ecology & Evolution, 20(1), 23–27. DOI: https://doi.org/10.1016/j.tree.2004.11.005

Guariguata, M. R., & Dupuy, J. M. (1997). Forest Regeneration in Abandoned Logging Roads in Lowland Costa Rica 1. Biotropica, 29(1), 15–28. DOI: https://doi.org/10.1111/j.1744-7429.1997.tb00002.x

Hanson, P. E. (2011). Insect diversity in seasonally dry tropical forests. In R. Dirzo, H.S. Young, H.A. Mooney, G. Ceballos (Eds.), Seasonally dry tropical forests (pp. 71–84). Island Press. DOI: https://doi.org/10.5822/978-1-61091-021-7_5

Heinen, J. T. (1992). Comparisons of the leaf litter herpetofauna in abandoned cacao plantations and primary rain forest in Costa Rica: some implications for faunal restoration. Biotropica, 24(3) 431–439. DOI: https://doi.org/10.2307/2388614

Heino, J. (2010). Are indicator groups and cross-taxon congruence useful for predicting biodiversity in aquatic ecosystems? Ecological Indicators, 10(2), 112–117. DOI: https://doi.org/10.1016/j.ecolind.2009.04.013

Hernández, H. A., & Barrera, A. E. P. (2018). Validación de un instrumento de investigación para el diseño de una metodología de autoevaluación del sistema de gestión ambiental. Revista de investigación agraria y ambiental, 9(1), 157–164. DOI: https://doi.org/10.22490/21456453.2186

Hess, G. R., Bartel, R. A., Leidner, A. K., Rosenfeld, K. M., Rubino, M. J., Snider, S. B., & Ricketts, T. H. (2006). Effectiveness of biodiversity indicators varies with extent, grain, and region. Biological conservation, 132(4), 448–457. DOI: https://doi.org/10.1016/j.biocon.2006.04.037

Hilje, B., Calvo-Alvarado, J., Jiménez-Rodríguez, C., & Sánchez-Azofeifa, A. (2015). Tree species composition, breeding systems, and pollination and dispersal syndromes in three forest successional stages in a tropical dry forest in Mesoamerica. Tropical Conservation Science, 8(1), 76–94. DOI: https://doi.org/10.1177/194008291500800109

Hilje, B., Sánchez, N. V., Bayne, E. M., & Sánchez-Azofeifa, A. (2020). Bird assemblage recovery in a chronosequence of tropical dry forests in Costa Rica. Forests, 11(6), 629. DOI: https://doi.org/10.3390/f11060629

Hodgson, J. A., Moilanen, A., Wintle, B. A., & Thomas, C. D. (2011). Habitat area, quality and connectivity: striking the balance for efficient conservation. Journal of Applied Ecology, 48(1), 148–152. DOI: https://doi.org/10.1111/j.1365-2664.2010.01919.x

Hodkinson, I. D., & Jackson, J. K. (2005). Terrestrial and aquatic invertebrates as bioindicators for environmental monitoring, with particular reference to mountain ecosystems. Environmental Management, 35(5), 649–666. DOI: https://doi.org/10.1007/s00267-004-0211-x

Hubbell, S. P., & Foster, R. B. (1983). Diversity of canopy trees in a neotropical forest and implications for conservation. In S. L. Sutton, T. C. Whitmore, & A. C. Chadwick (Eds.), Tropical rainforest: ecology and management (pp. 25–41). Blackwell Scientific Publications.

Hubbell, S. P., Foster, R. B., O’Brien, S. T., Harms, K. E., Condit, R., Wechsler, B., Wryght, S. J., & De Lao, S. L. (1999). Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science, 283(5401), 554–557. DOI: https://doi.org/10.1126/science.283.5401.554

Hurtt, G. C., & Pacala, S. W. (1995). The consequences of recruitment limitation: reconciling chance, history and competitive differences between plants. Journal of Theoretical biology, 176(1), 1–12. DOI: https://doi.org/10.1006/jtbi.1995.0170

Janzen, D. H. (1988). Tropical dry forests. Biodiversity, 15, 130–137.

Janzen, D. H., & Hallwachs, W. (2021). To us insectometers, it is clear that insect decline in our Costa Rican tropics is real, so let’s be kind to the survivors. Proceedings of the National Academy of Sciences, 118(2), 1–8. DOI: https://doi.org/10.1073/pnas.2002546117

Kasso, M., & Balakrishnan, M. (2013). Ecological and economic importance of bats (Order Chiroptera). International Scholarly Research Notices, 2013, 1–9. DOI: https://doi.org/10.1155/2013/187415

Kati, V., Devillers, P., Dufrêne, M., Legakis, A., Vokou, D., & Lebrun, P. (2004). Testing the value of six taxonomic groups as biodiversity indicators at a local scale. Conservation biology, 18(3), 667–675. DOI: https://doi.org/10.1111/j.1523-1739.2004.00465.x

Kerr, J. T. (1997). Species richness, endemism, and the choice of areas for conservation: Riqueza de Especies, Endemismo y Selección de Areas para Conservación. Conservation Biology, 11(5), 1094–1100. DOI: https://doi.org/10.1046/j.1523-1739.1997.96089.x

Lacher Jr, T. E., Davidson, A. D., Fleming, T. H., Gómez-Ruiz, E. P., McCracken, G. F., Owen-Smith, N., ... & Vander Wall, S. B. (2019). The functional roles of mammals in ecosystems. Journal of Mammalogy, 100(3), 942–964. DOI: https://doi.org/10.1093/jmammal/gyy183

Lambeets, K., Vandegehuchte, M. L., Maelfait, J. P., & Bonte, D. (2008). Understanding the impact of flooding on trait‐displacements and shifts in assemblage structure of predatory arthropods on river banks. Journal of animal Ecology, 77(6), 1162–1174. DOI: https://doi.org/10.1111/j.1365-2656.2008.01443.x

Laurila-Pant, M., Lehikoinen, A., Uusitalo, L., & Venesjärvi, R. (2015). How to value biodiversity in environmental management? Ecological indicators, 55, 1–11. DOI: https://doi.org/10.1016/j.ecolind.2015.02.034

LaVal, R. K., & Rodríguez, B. (2002). Costa Rica bats. Editorial INBio. San José, Costa Rica.

Legendre, P., Borcard, D., & Peres-Neto, P. R. (2005). Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecological monographs, 75(4), 435–450. DOI: https://doi.org/10.1890/05-0549

Lieberman, D., Lieberman, M., Peralta, R., & Hartshorn, G. S. (1985). Mortality patterns and stand turnover rates in a wet tropical forest in Costa Rica. The Journal of Ecology, 915–924. DOI: https://doi.org/10.2307/2260157

Lindenmayer, D. B., Margules, C. R., & Botkin, D. B. (2000). Indicators of biodiversity for ecologically sustainable forest management. Conservation Biology, 14(4), 941–950. DOI: https://doi.org/10.1046/j.1523-1739.2000.98533.x

Lovell, S., Hamer, M., Slotow, R., & Herbert, D. (2007). Assessment of congruency across invertebrate taxa and taxonomic levels to identify potential surrogates. Biological Conservation, 139(1-2), 113–125. DOI: https://doi.org/10.1016/j.biocon.2007.06.008

Lukacs, P. (2009). Closed population capture-recapture models. In E. Cooch (Eds.), Program MARK: a gentle introduction, (pp. 14.1–14.61). University of Montana.

Lund, M. P., & Rahbek, C. (2002). Cross-taxon congruence in complementarity and conservation of temperate biodiversity. Animal Conservation forum, 5(2), 163–171. DOI: https://doi.org/10.1017/S1367943002002226

Majer, J. D., Delabie, J. H. C., & McKenzie, N. L. (1997). Ant litter fauna of forest, forest edges and adjacent grassland in the Atlantic rain forest region of Bahia, Brazil. Insectes Sociaux, 44(3), 255–266. DOI: https://doi.org/10.1007/s000400050046

Massolo, L. A. (2015). Introducción a las herramientas de gestión ambiental. Series: Libros de Cátedra. http://sedici.unlp.edu.ar/bitstream/handle/10915/46750/Documento_completo__.pdf%3Fsequence%3D1 DOI: https://doi.org/10.35537/10915/46750

McGeoch, M. A. (1998). The selection, testing and application of terrestrial insects as bioindicators. Biological reviews, 73(2), 181–201. DOI: https://doi.org/10.1017/S000632319700515X

McKenney, B., Kiesecker, J. (2009). Policy development for biodiversity offsets: a review of offset frameworks. Environmental Management, 45(1) 165–176. DOI: https://doi.org/10.1007/s00267-009-9396-3

Menkhorst, P., Clemann, N., & Sumner, J. (2016). Fauna-rescue programs highlight unresolved scientific, ethical and animal welfare issues. Pacific Conservation Biology, 22(4), 301–303. DOI: https://doi.org/10.1071/PC16007

Moreno, C. E., Sánchez-Rojas, G., Pineda, E., & Escobar, F. (2007). Shortcuts for biodiversity evaluation: a review of terminology and recommendations for the use of target groups, bioindicators and surrogates. International Journal of Environment and Health, 1(1), 71–86. DOI: https://doi.org/10.1504/IJENVH.2007.012225

Nally, R. M., & Fleishman, E. (2004). A successful predictive model of species richness based on indicator species. Conservation biology, 18(3), 646–654. DOI: https://doi.org/10.1111/j.1523-1739.2004.00328_18_3.x

Neuschulz, E. L., Mueller, T., Schleuning, M., & Böhning-Gaese, K. (2016). Pollination and seed dispersal are the most threatened processes of plant regeneration. Scientific Reports, 6(1), 1–6. DOI: https://doi.org/10.1038/srep29839

Norden, N., Chave, J., Caubere, A., Chatelet, P., Ferroni, N., Forget, P. M., & Thébaud, C. (2007). Is temporal variation of seedling communities determined by environment or by seed arrival? A test in a neotropical forest. Journal of Ecology, 95(3), 507–516. DOI: https://doi.org/10.1111/j.1365-2745.2007.01221.x

Nussear, K. E., Tracy, C. R., Medica, P. A., Wilson, D. S., Marlow, R. W., & Corn, P. S. (2012). Translocation as a conservation tool for Agassiz’s desert tortoises: survivorship, reproduction, and movements. The Journal of Wildlife Management, 76(7), 1341–1353. DOI: https://doi.org/10.1002/jwmg.390

O’Riordan, T. (2014). Environmental Science for Environmental Management. Routledge https://www.taylorfrancis.com/books/mono/10.4324/9781315839592/environmental-science-environmental-management-timothy-riordan

Ovadia, O. (2003). Ranking hotspots of varying sizes: A lesson from the nonlinearity of the species-area relationship. Conservation Biology, 17(5), 1440–1441. DOI: https://doi.org/10.1046/j.1523-1739.2003.02066.x

Paoletti, M. G. (1999). Using bioindicators based on biodiversity to assess landscape sustainability. In M.G. Paoletti (Eds.), Invertebrate biodiversity as bioindicators of sustainable landscapes (pp. 1–18). Elsevier. DOI: https://doi.org/10.1016/B978-0-444-50019-9.50004-2

Parkes, D., Newell, G., & Cheal, D. (2003). Assessing the quality of native vegetation: the ‘habitat hectares’ approach. Ecological Management & Restoration, 4(1), S29–S38. DOI: https://doi.org/10.1046/j.1442-8903.4.s.4.x

Pearson, D. L., & Carroll, S. S. (1998). Global patterns of species richness: spatial models for conservation planning using bioindicator and precipitation data. Conservation biology, 12(4), 809–821. DOI: https://doi.org/10.1111/j.1523-1739.1998.96460.x

Pearson, D. L., & Cassola, F. (1992). World-wide species richness patterns of tiger beetles (Coleoptera: Cicindelidae): indicator taxon for biodiversity and conservation studies. Conservation Biology, 6(3), 376–391. DOI: https://doi.org/10.1046/j.1523-1739.1992.06030376.x

Perevochtchikova, M. (2013). La evaluación del impacto ambiental y la importancia de los indicadores ambientales. Gestión y Política Pública, 22(2), 283–312.

Pérez, G. R. (1999). Los macroinvertebrados y su valor como indicadores de la calidad del agua. Academia Colombiana de Ciencia, 23(88), 375–387. DOI: https://doi.org/10.18257/raccefyn.23(88).1999.2870

Poder Ejecutivo. (1996, 15 de noviembre). Decreto 25700-MINAE. Declara veda total el aprovechamiento de árboles en peligro extinción. Diario Oficial La Gaceta. http://www.pgrweb.go.cr/scij/Busqueda/Normativa/Normas/nrm_texto_completo.aspx?param1=NRTC&nValor1=1&nValor2=29811&nValor3=108834&strTipM=TC

Poder Ejecutivo. (2017, 12 de julio). Decreto 40548. MINAE. Reglamento a Ley de Conservación de Vida Silvestre, Diario Oficial La Gaceta 150. http://www.pgrweb.go.cr/scij/Busqueda/Normativa/Normas/nrm_texto_completo.aspx?nValor1=1&nValor2=84592

Potts, M. D., Ashton, P. S., Kaufman, L. S., & Plotkin, J. B. (2002). Habitat patterns in tropical rain forests: a comparison of 105 plots in northwest Borneo. Ecology, 83(10), 2782–2797. DOI: https://doi.org/10.1890/0012-9658(2002)083[2782:HPITRF]2.0.CO;2

Powers, J. S., & Tiffin, P. (2010). Plant functional type classifications in tropical dry forests in Costa Rica: leaf habit versus taxonomic approaches. Functional Ecology, 24(4), 927–936. DOI: https://doi.org/10.1111/j.1365-2435.2010.01701.x

Powers, J. S., Becknell, J. M., Irving, J., & Perez-Aviles, D. (2009). Diversity and structure of regenerating tropical dry forests in Costa Rica: Geographic patterns and environmental drivers. Forest Ecology and Management, 258(6), 959–970. DOI: https://doi.org/10.1016/j.foreco.2008.10.036

Prieto-Torres, D. A., Rojas-Soto, O. R., Bonaccorso, E., Santiago-Alarcon, D., & Navarro-Sigüenza, A. G. (2019). Distributional patterns of Neotropical seasonally dry forest birds: a biogeographical regionalization. Cladistics, 35(4), 446–460. DOI: https://doi.org/10.1111/cla.12366

Quesada-Monge, R. (2004). Especies forestales vedadas y bajo otras categorías de protección en Costa Rica. Kurú: Revista Forestal 1(2), 1–5.

Quesada-Monge, R. (2008). Especies forestales vedadas en Costa Rica. In Actas del 10º Congreso Nacional de Ciencias y Estudios Sociales (pp 6). Universidad Nacional de Costa Rica.

Quetier, F., Lavorel, S. (2011). Assessing ecological equivalence in biodiversity offset schemes: Key issues and solutions. Biological Conservation 144, 2991–2999. DOI: https://doi.org/10.1016/j.biocon.2011.09.002

Reid, W. V. (1998). Biodiversity hotspots. Trends in Ecology & Evolution, 13(7), 275–280. DOI: https://doi.org/10.1016/S0169-5347(98)01363-9

Restello, R. M. & A. M. Penteado-Dias. (2006). Diversidade dos Braconidae (Hymenoptera) da Unidade de Conservação de Teixeira Soares, Marcelino Ramos, RS, com ênfase nos Microgastrinae. Revista Brasileira de Entomologia 50, 80–84. DOI: https://doi.org/10.1590/S0085-56262006000100012

Ricketts, T. H., Dinerstein, E., Olson, D. M., Eichbaum, W., Loucks, C. J., DellaSala, D. A., Kavanagh, K., Heda, P., Hurley, P. T., Carney, K. M., Abell., R., & Walters, S. (1999). Terrestrial ecoregions of North America: a conservation assessment (Vol. 1). Island Press.

Rodrigues, A. S., Akcakaya, H. R., Andelman, S. J., Bakarr, M. I., Boitani, L., Brooks, T. M., Chanson, J.S., Fishpool, L. D. C., Da Fonseca, G. A. B., Gaston, K. J., Hoffmann, M, Marquet, P. A., Pilgrim, J. D., Pressey, R. L., Schipper, J., Sechrest, E., Stuart, S. N., Underhill, L. G., Waller, R. W., Watts, M. E. J. & Yan, X. (2004). Global gap analysis: priority regions for expanding the global protected-area network. BioScience, 54(12), 1092–1100. DOI: https://doi.org/10.1641/0006-3568(2004)054[1092:GGAPRF]2.0.CO;2

Rodríguez-Herrera, B., J. D. Ramírez-Fernández, D. Villalobos-Chaves y R. Sánchez. (2014). Actualización de la lista de especies de mamíferos vivientes de Costa Rica. Mastozoología Neotropical, 21(2), 275–289.

Rosenberg, D. M., Danks, H. V., & Lehmkuhl, D. M. (1986). Importance of insects in environmental impact assessment. Environmental management, 10(6), 773–783. DOI: https://doi.org/10.1007/BF01867730

Saetersdal, M., Line, J. M., & Birks, H. J. B. (1993). How to maximize biological diversity in nature reserve selection: vascular plants and breeding birds in deciduous woodlands, western Norway. Biological Conservation, 66(2), 131–138. DOI: https://doi.org/10.1016/0006-3207(93)90144-P

Sasa, M., & Bolaños. F. (2004). Biodiversity and conservation of Mesoamerican dry forest herpetofauna. In G. Frankie, & A. Mata (Eds.), Diversity and Conservation of Costa Rican Dry Forest (pp. 177–193). U C Press, California. DOI: https://doi.org/10.1525/california/9780520223097.003.0014

Sasa, M., Chaves, G., & Porras L. W. (2010). The Costa Rican herpetofauna: Conservation status and future perspectives. In L. D. Wilson, J. H. Townsend, & J. D. Johnson (Eds.), Conservation of Mesoamerican Amphibians and Reptiles (pp. 509–603). Eagle Mountain Publications.

Sandlund, O. T., Daverdin, R., Choudhury, A., Brooks, D. R., & Diserud, O. H. (2010). A survey of freshwater fishes and their macroparasites in the Guanacaste Conservation Area (ACG), Costa Rica. NINA Report, 635.

Savage, J. M. (2002). The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago press.

Shimadzu, H. (2018). On species richness and rarefaction: size-and coverage-based techniques quantify different characteristics of richness change in biodiversity. Journal of Mathematical Biology, 77(5), 1363–1381. DOI: https://doi.org/10.1007/s00285-018-1255-5

Silva Chaves, L. D., Caselli, C. B., Albuquerque Carvalho, R. D., & Alves, R. R. N. (2019). Noninvasive Sampling Techniques for Vertebrate Fauna. In U. Albuquerque, R. de Lucena, L. Cruz da Cunha, & R. Alves (Eds.), Methods and Techniques in Ethnobiology and Ethnoecology (pp. 309–321). Humana Press, New York, NY. DOI: https://doi.org/10.1007/978-1-4939-8919-5_20

Simberloff, D. (1998). Flagships, umbrellas, and keystones: is single-species management passé in the landscape era? Biological conservation, 83(3), 247–257. DOI: https://doi.org/10.1016/S0006-3207(97)00081-5

Sisson, D. C., Palmer, W. E., Terhune, T. M., & Thackston, R. E. (2012). Development and implementation of a successful northern bobwhite translocation program in Georgia. National Quail Symposium Proceedings 7(1), 111. DOI: https://doi.org/10.7290/nqsp0758cn

Soberón, J. M., Llorente, J. B., & Oñate, L. (2000). The use of specimen-label databases for conservation purposes: an example using Mexican Papilionid and Pierid butterflies. Biodiversity & conservation, 9(10), 1441–1466. DOI: https://doi.org/10.1023/A:1008987010383

Stoner, K. E., & Timm, R. M. (2004). Tropical dry-forest mammals of Palo Verde: Ecology and conservation in a changing landscape. In G. Frankie, & A. Mata (Eds.), Diversity and Conservation of Costa Rican Dry Forest (pp. 48–66). U C Press, California. DOI: https://doi.org/10.1525/california/9780520223097.003.0005

Stork, N. E. (1988). Insect diversity: facts, fiction and speculation. Biological journal of the Linnean Society, 35(4), 321–337. DOI: https://doi.org/10.1111/j.1095-8312.1988.tb00474.x

Ten Kate, K., Bishop, J., & Bayon, R. (2004). Biodiversity offsets: Views, experience, and the business case. IUCN, Gland, Switzerland and Cambridge, UK and Insight Investment.

Terborgh, J., Foster, R. B., & Percy, N. V. (1996). Tropical tree communities: a test of the nonequilibrium hypothesis. Ecology, 77(2), 561–567. DOI: https://doi.org/10.2307/2265630

Tilman, D., & Pacala, S. (1993). The maintenance of species richness in plant communities. Unknown Journal, 13–25.

Tonkin, J. D., Death, R. G., & Collier, K. J. (2013). Do productivity and disturbance interact to modulate macroinvertebrate diversity in streams? Hydrobiologia, 701(1), 159–172. DOI: https://doi.org/10.1007/s10750-012-1248-0

Turley, N. J., & Holthuijzen, A. M. (2005). Impact of a catastrophic flooding event on riparian birds. Western North American Naturalist, 65(2), 274–277.

UICN--The World Conservation Union, Unión Internacional para la Conservación de la Naturaleza, de los Recursos Naturales, Comisión de Supervivencia de Especies de la UICN., & IUCN Species Survival Commission. (2001). Categorías y criterios de la Lista Roja de la UICN, versión 3.1. IUCN. https://www.iucnredlist.org/

Urbina-Cardona, J. N., Olivares-Pérez, M., & Reynoso, V. H. (2006). Herpetofauna diversity and microenvironment correlates across a pasture–edge–interior ecotone in tropical rainforest fragments in the Los Tuxtlas Biosphere Reserve of Veracruz, Mexico. Biological conservation, 132(1), 61–75. DOI: https://doi.org/10.1016/j.biocon.2006.03.014

Van Bael, S. A., Bichier, P., Ochoa, I., & Greenberg, R. (2007). Bird diversity in cacao farms and forest fragments of western Panama. Biodiversity and Conservation, 16(8), 2245–2256. DOI: https://doi.org/10.1007/s10531-007-9193-3

Van Jaarsveld, A. S., Biggs, R., Scholes, R. J., Bohensky, E., Reyers, B., Lynam, T., Musvoto, C. & Fabricius, C. (2005). Measuring conditions and trends in ecosystem services at multiple scales: the Southern African Millennium Ecosystem Assessment (SA f MA) experience. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1454), 425–441. DOI: https://doi.org/10.1098/rstb.2004.1594

Vera, P., Sasa, M., Encabo, S. I., Barba, E., Belda, E. J., & Monrós, J. S. (2011). Land use and biodiversity congruences at local scale: applications to conservation strategies. Biodiversity and Conservation, 20(6), 1287–1317. DOI: https://doi.org/10.1007/s10531-011-0028-x

White, G. C. (1982). Capture-recapture and removal methods for sampling closed populations. Los Alamos National Laboratory.

Wilson, L. D., & McCranie J.R. (1992). Status of amphibian populations in Honduras. Unpublished Report to the Task Force on Declining Amphibian Populations.

Wilson, L. D., & McCranie, J. R. (2004). The conservation status of the herpetofauna of Honduras. Amphibian and Reptile Conservation, 3(1), 6.

Wolters, V., Bengtsson, J., & Zaitsev, A. S. (2006). Relationship among the species richness of different taxa. Ecology, 87(8), 1886–1895. DOI: https://doi.org/10.1890/0012-9658(2006)87[1886:RATSRO]2.0.CO;2

Zhang, Y., Li, Z., Ge, W., Wang, J., Guo, X., Wang, T., & Li, W. (2022). Assessment of the impact of floods on terrestrial plant biodiversity. Journal of Cleaner Production, 339, 130722. DOI: https://doi.org/10.1016/j.jclepro.2022.130722

Published

2022-12-15