Revista Facultad Nacional de Agronomía Medellín
0304-2847
Facultad de Ciencias Agrarias - Universidad Nacional de Colombia
https://doi.org/10.15446/rfna.v71n2.66113

Recibido: 5 de julio de 2017; Aceptado: 24 de enero de 2018

Contribution of agroecosystems to the conservation of bird diversity in the department of Caldas

Aporte de los agroecosistemas a la conservación de la diversidad de las aves silvestres en el departamento de Caldas

E. Martínez-Sánchez, 1M. Cardona-Romero, 1F. Rivera-Páez, 1J. Pérez-Cárdenas, 2G. Castaño-Villa, 3

1 Facultad de Ciencias Exactas y Naturales. Universidad de Caldas. AA 275, Manizales, Colombia. <estefani.1711110222@ucaldas.edu.co> Universidad de Caldas Facultad de Ciencias Exactas y Naturales Universidad de Caldas Manizales Colombia
2 Facultad de Ciencias para la Salud. Universidad de Caldas. AA 275, Manizales, Colombia. Universidad de Caldas Facultad de Ciencias para la Salud Universidad de Caldas Manizales Colombia
3 Facultad de Ciencias Agropecuarias. Universidad de Caldas. AA 275, Manizales, Colombia. Universidad de Caldas Facultad de Ciencias Agropecuarias Universidad de Caldas Manizales Colombia

ABSTRACT

In tropical regions, the contributions and limitations of agroecosystems have been identified with respect to bird diversity conservation. It has been suggested that agroecosystems can have different conservation values, according to the structural complexity of the vegetation (e.g., higher number of vegetation strata, cultivated species diversity, among others). Therefore, agroecosystems, especially those with a smaller area (e.g., small-holdings), could be crucial for developing bird conservation strategies. In order to establish the contribution of different agroecosystem types to bird conservation in the department of Caldas (Colombia), we compared bird richness, abundance, and similarity associated to three types of habitats: (1) type I agroecosystems (mono-cropping with bare soil), (2) type II agroecosystems (mixed-cropping, grazing pastures with weeds and dispersed trees, and plantations with understory), and (3) secondary forests. Type II agroecosystems did not differ in bird richness and similarity compared to secondary forests, and species with high sensitivity to disturbance were registered (Zentrygon frenata, Phaetornis guy, Phaetornis syrmatophorus, Lepidocolaptes lacrymiger and Sphenopsis frontalis). Additionally, we registered a species of global conservation interest (Chloropipo flavicapilla) and four migratory species (Catharus ustulatus, Parkesia noveboracensis, Setophaga fusca and Setophaga striata) in this type of agroecosystem. Thus, type II agroecosystem habitats are not completely negative on avifauna, and they could serve an important role within conservation strategies in rural landscapes.

Keywords:

Avifauna, Secondary forests, Structural complexity of the vegetation, Mixed-cropping, Mono-cropping, Plantations.

RESUMEN

En las regiones tropicales se han identificado los aportes y limitaciones de los agroecosistemas en el contexto de la conservación de la diversidad de las aves. Se ha sugerido que los agroecosistemas pueden presentar un valor diferente para la conservación, de acuerdo con la complejidad estructural de la vegetación (e.g., mayor número de estratos de la vegetación, diversidad de las especies cultivadas, entre otros). En este sentido, los agroecosistemas de una menor área (e.g., minifundios), pueden ser claves en el desarrollo de estrategias encaminadas a la conservación de la avifauna. Con el objetivo de establecer el aporte de diferentes tipos de agroecosistemas a la conservación de las aves en el departamento de Caldas (Colombia), se comparó la riqueza, abundancia y similitud de las aves asociadas a tres tipos de hábitats: (1) agroecosistemas tipo I (monocultivos con suelo limpio), (2) agroecosistemas tipo II (cultivos mixtos, potreros enmalezados con árboles dispersos y plantaciones con sotobosque) y (3) bosques secundarios. Los agroecosistemas tipo II no difirieron en la riqueza y en la similitud de las aves con respecto a los bosques secundarios, además se registraron especies con alta sensibilidad a la perturbación (Zentrygon frenata, Phaetornis guy, Phaetornis syrmatophorus, Lepidocolaptes lacrymiger y Sphenopsis frontalis). Adicionalmente en este tipo de agroecosistemas se registró una especie de interés para la conservación global (Chloropipo flavicapilla) y cuatro especies migratorias (Catharus ustulatus, Parkesia noveboracensis, Setophaga fusca y Setophaga striata). Los agroecosistemas tipo II no son hábitats completamente negativos para la avifauna y podrían desempeñar un rol importante dentro de las estrategias para la conservación en paisajes rurales.

Palabras clave:

Avifauna, Bosques secundarios, Complejidad estructural de la vegetación, Cultivos mixtos, Monocultivos, Plantaciones.

Agroecosystems cover approximately 28% of the arable land surface; 31% of which is occupied by crops and the remaining 69% by low pastures (Wood et al., 2000). In particular, approximately 61% of the arable area is found in tropical regions (Wood et al., 2000), which contain most of the biodiversity of the planet (Gentry, 1992). In the next 30 years, a 13% increase in the area covered by agroecosystems will be necessary, prompted by the increasing demand of space for the production of food, wood, and other goods and services (Sala et al., 2000; Bruinsma, 2003). It is known, though, that land use change (e.g., conversion of native forests to agroecosystems) is an important driver of global species extinctions (Díaz et al., 2006; Dent and Wright, 2009); while, native forests are clearly fundamental for biodiversity conservation in the tropical region (Chazdon et al., 2009; Gibson et al., 2011). However, some agroecosystems could be contributing to conservation, since they contain several elements of the biodiversity found in forests (Castaño-Villa et al., 2008; Gibson et al., 2011), and the presence of wildlife in agroecosystems represents an opportunity to incorporate these lands into conservation plans (Simonetti et al., 2012).

In this context, diverse studies in the Tropics have identified the contribution and limitations of agroecosystems (e.g., forest, cocoa, coffee plantations, among others) for bird diversity conservation (Faria et al., 2006; Barlow et al., 2007; Philpott and Bichier, 2012). The structural complexity of the vegetation within an agroecosystem (e.g., higher number of vertical strata) is a key factor that can promote the use of these habitats by birds, including those associated to native forests (Nájera and Simonetti 2010; Castaño-Villa et al., 2014; Vergara-Paternina et al., 2017). However, few studies have considered the importance of bird diversity conservation in agroecosystems at a smaller spatial scale in rural landscapes, such as smallholding agroecosystems (Petit and Petit, 2003; Cárdenas et al., 2003). Rural landscapes cover 62% of the Colombian Andes (Arango et al., 2003) and these are considered a key element in the development of biodiversity conservation strategies (Lozano-Zambrano et al., 2009).

The department of Caldas presents the greatest habitat transformation rates, as well as 48% of the Colombian bird diversity (Corporación Autónoma Regional de Caldas y Asociación Calidris, 2010; Corpocaldas, 2016). This poses an ideal setting to assess the value of different agroecosystems for bird diversity conservation. Accordingly, this study compared avifauna associated to agroecosystems and secondary forests of the department of Caldas, with the aim of establishing the contribution of different agroecosystem types to bird conservation. Our hypothesis is that agroecosystems with a greater structural complexity of the vegetation contain some bird species associated to native forests, and consequently, contribute to the conservation of this group.

MATERIALS AND METHODS

Study area

The department of Caldas is located in the central west Andes of Colombia (4°4'19”N; 75°57'26”W). It is composed of mountainous areas belonging to the Central and Western Andes Mountain Ranges and the inter-Andean valleys of the Cauca and Magdalena Rivers. The department covers a surface area of 7457 km2, with an altitudinal range between 140 to 5350 m of altitude. It presents an annual precipitation average of 2800 mm, with two rainy seasons (March - June and September - December) and two less rainy periods (January - February and July - August), and a temperature that varies from 13 °C - 27 °C (Jaramillo-Robledo et al., 2011). In Caldas, agriculture spans 69.26% of the territory, with seasonal and permanent crops, while 21.88% is covered by native and/or planted forests. Coffee (Coffea arabica L.) is the main productive system in the department, followed in order of economic importance by plantain (Musa sp.), fruit trees (citric), and cocoa (Theobroma cacao L.) (Ministerio de Agricultura y Desarrollo Rural, 2006). In order to encompass this environmental diversity, we conducted bird surveys in 11 municipalities of the department: Pácora, Victoria, Samaná, Pensilvania, Manizales, Palestina, Chinchiná, Villamaría, Marmato, Riosucio, and San José, throughout an altitudinal range of 551 to 2679 m.

Habitats Selection

For sampling habitats selection, we used images from Google Earth version 7.1. Three types of habitats were selected from the images: type I agroecosystems (ATI, n=8), type II (ATII, n=5), and secondary forests (SF, n=8) (Figure 1). Eight habitats were defined as type I agroecosystems, namely mono-cropping with bare soil (ATI1: cocoa; ATI2: avocado; ATI3: lemon; ATI4: pasture; ATI5: papaya; ATI6: citric; ATI7-8: coffee; Table 1). Five habitats were assigned as type II agroecosystems, including mixed-cropping, grazing pastures with dispersed trees, and forest plantations with developed understory (ATII1: corn, cassava, plantain, and forage species; ATII2: coffee and plantain; ATII3: grazing pastures with weeds and dispersed tree cover; ATII4: urapán (Fraxinus chinensis) plantation; and ATII5: patula pine (Pinus patula) plantation; Table 1). Finally, eight secondary forests were also selected (SF1-SF8; Table 1). All of the selected agroecosystems were located at a distance no greater than 245 m from a secondary forest. The distance between agroecosystems varied from 10 to 120 km, except for ATI5 and ATI6 that were located in the same sampling site. A detailed description of each habitat is given in Table 1. All agroecosystems included a secondary forest (control) within the same site.

Map of the sampling habitat types in the department of Caldas, Colombia. ATI (type I agroecosystems); ATII (type II agroecosystems); SF (secondary forests).

Figure 1: Map of the sampling habitat types in the department of Caldas, Colombia. ATI (type I agroecosystems); ATII (type II agroecosystems); SF (secondary forests).

Table 1: Habitat description (type I and II agroecosystems and secondary forests) of avifauna of the department of Caldas.

Bird capture

The avifauna present in each habitat type (type I and II agroecosystems and secondary forests) was assessed by mist net sampling, which has been previously used in agroecosystem and secondary forest studies (Blake and Loiselle, 2001; Barlow et al., 2007; Castaño-Villa et al., 2014). Between November to December of 2015 and January to April of 2016, we established 12 capture points within each site, and at each point, a mist net (12 × 2.5 m × 36 mm) was extended for 10 hours. The nets were randomly installed at each site and operated between 600 h and 1730 h. Each site was visited for four to five days until completing 120-net hours. Within each habitat type, mist nets were extended in an area of 0.1 ha. The total sampling effort for ATI was 960-net hours, 600-net hours for ATII, and 960-net hours for SF. The nets were not operated under rainfall, wind, or intense cold or heat. The birds captured were individualized through a small cut on the first tail rectrix in order to prevent counting more than once, and then released in the capture site. Birds were identified using the identification guide of Birds of Northern South America (Restall et al., 2007). Taxonomic classification of bird species was done according to Remsen et al. (2017).

Data analysis

We compared species richness, abundance and similarity between the two agroecosystem types and their corresponding secondary forests, in order to describe the contribution of agroecosystems to avifauna conservation. Species were categorized based on the criterion of sensitivity to disturbance (high, moderate, low), according to Stotz et al. (1996). Species with a high sensitivity to disturbance are known to be most affected by anthropogenic habitat modification (Castaño-Villa et al., 2014), so they are considered vulnerable and relevant to conservation at a local level. To determine if bird species richness statistically differed between the three habitats studied, we graphed lower and upper confidence intervals at 84% of the estimated species richness (S est), using Mao Tao SD values, according to MacGregor-Fors and Payton (2013) and subsequent applications (Hanula et al., 2015; Fontúrbel et al., 2016). Mao Tao SD values were obtained from rarefaction analysis using EstimateS version 9.1.0 (Colwell, 2013). When the confidence intervals did not overlap, these were considered statistically significantly different with an alpha of 0.05. We considered the capture points within each site to be replicas (12 points per site). Habitats were compared by the same number of replicates (60), which was the minimum number of replicates obtained for ATII. Additionally, observed species richness was compared between type I and II agroecosystems, according to sensitivity to disturbance, through Fisher's Exact Test. The number of individuals captured within each habitat (i.e. abundance of all species captured, standardized for the sampling effort), shown as medians, was compared through of a Generalized Linear Model (Poisson distribution). Abundance data referred to the number of captures, not to real abundance, which is unknown. The differences in bird assemblage similarity (in terms of species abundance) between habitats were assessed by a One-Way Analysis of Similarity (ANOSIM), which constitutes a non-parametric permutation test (Clarke, 1993). For this analysis, a Bray-Curtis distance was used, which has been previously used in other studies to compare bird assemblages (Barlow et al., 2007; Castaño-Villa et al., 2014). The ANOSIM test was carried out with PAST 2.15 (Hammer et al., 2001). Additionally, we used a Non-metric Multidimensional Scaling analysis (NMDS) to visualize differences in the composition among habitat types. GLM and NMDS analyses were carried out on R version 3.4.3 (R Development Core Team, 2017).

RESULTS AND DISCUSSION

We captured 538 birds in the three habitats, belonging to 139 species from 24 families; type I agroecosystems (S=72), type II (S=59), and secondary forests (S=70). From those, 14 bird species were captured in the three habitat types (Table 2). Estimated bird species richness (S est) shows a wide variation among all sampling sites (Figure 2a). Within type I agroecosystems, citric crops (ATI6) showed the highest estimated species richness (S est=21), while the grazing pasture with weeds and dispersed trees (ATII3) showed the highest estimated richness (S est=24) among type II agroecosystems. Estimated birds richness was 58.62 (ATI), 59.00 (ATII), and 52.66 (SF) for a similar sampling effort. No significant differences in S est were found between the three habitats (Figure 2b). Regarding sensitivity to habitat disturbance, highly vulnerable species were not captured in type I agroecosystems, while in type II, five species with this characteristic were registered (Zentrygon frenata, Phaetornis guy, Phaetornis syrmatophorus, Lepidocolaptes lacrymiger, and Sphenopsis frontalis). Similar results have been reported for other agroecosystems, which have shown that structural complexity of the vegetation (e.g., higher number of vegetation strata, cultivated species diversity, among others) could possibly offer a greater variety of microhabitats and resources used by birds, including those typical of forests (Greenberg et al., 1997; Petit et al., 1999; Petit and Petit, 2003; Nájera and Simonetti 2010; Díaz-Bohórquez et al., 2014). However, mixed-cropping (included in type II agroecosystems) harbor low species richness compared to the other agroecosystems assessed herein, which could be attributed to its rotational nature that does not allow long term bird species establishment (Petit and Petit, 2003) (ATII1, Figure 2a). The number of species with moderate sensitivity to disturbance found in type I and II agroecosystems was 12 in both cases, belonging to the families Trochilidae, Furnariidae, Tyrannidae, Turdidae, Thraupidae, Emberizidae and Parulidae (Table 2). Accordingly, observed species richness, based on sensitivity to disturbance, differed between type I and type II agroecosystems (Fisher's Exact Test, P=0.02). Overall, it seems likely that type II agroecosystems, surrounded by native forests and areas such as the ones described in this study, are not completely negative on avifauna. In respect, agroecosystem bird diversity is favored when native forest surrounding to agroecosystem, because the landscape heterogeneity can favor the diversity of this group (Lindenmayer and Hobbs, 2004; Gardner et al., 2009).

Table 2: Sensitivity to disturbance and habitat type of the bird species.

Estimated species richness (S est), A. for all habitats sampled, ATI1: cocoa; ATI2: avocado; ATI3: lemon; ATI4: pasture; ATI5: papaya; ATI6: citric; ATI7-8: coffee; ATII1: cassava, plantain and forage species; ATII2: coffee and plantain; ATII3: grazing pasture with weeds and dispersed trees; ATII4: urapán plantation; and ATII5: patula pine plantation. SF1-SF8: secondary forests; B. for the three habitat types. ATI (type I agroecosystems); ATII (type II agroecosystems); SF (secondary forests).

Figure 2: Estimated species richness (S est), A. for all habitats sampled, ATI1: cocoa; ATI2: avocado; ATI3: lemon; ATI4: pasture; ATI5: papaya; ATI6: citric; ATI7-8: coffee; ATII1: cassava, plantain and forage species; ATII2: coffee and plantain; ATII3: grazing pasture with weeds and dispersed trees; ATII4: urapán plantation; and ATII5: patula pine plantation. SF1-SF8: secondary forests; B. for the three habitat types. ATI (type I agroecosystems); ATII (type II agroecosystems); SF (secondary forests).

Bird abundance for each of the habitats assessed was 27.50 (ATI), 18.00 (ATII), and 19.00 (SF), with significant differences found among these (P<0.05). A similar result was found when we compared the abundance of birds with moderate and low sensitivity to disturbance among the three habitats (P<0.05). Finally, differences in similarity were found between type I agroecosystems and secondary forests (ANOSIM, r=0.26; P=0.01), and not between type II agroecosystems and secondary forests (ANOSIM, r=0.12; P=0.16) (Figure 3). The differences in the abundance and species composition between agroecosystem and secondary forest can be explained by the greater abundance of typical birds of open and disturbed areas present in the agroecosystem, not found in the secondary forest (Bellocq et al., 2011). Although birds associated with agroecosystem type I are less relevant to conservation, these birds carry out important functions within agroecosystems, by controlling pests, pollinizers, and seed dispersers (Pejchar et al., 2008; Gardner et al., 2009; Philpott and Bichier, 2012).

Non-metric Multidimensional Scaling Analysis (NMDS). All habitats sampled, ATI (type I agroecosystems); ATII (type II agroecosystems); SF (secondary forests).

Figure 3: Non-metric Multidimensional Scaling Analysis (NMDS). All habitats sampled, ATI (type I agroecosystems); ATII (type II agroecosystems); SF (secondary forests).

Furthermore, in type I and type II agroecosystems, two endemic species of Colombia were found, Capito hypoleucus and Chloropipo flavicapilla. These two species are classified as Vulnerable (VU), due to reductions in their population sizes (International Union for Conservation of Nature, 2016). Finally, 14 migratory boreal species were registered in the type I and II agroecosystems, some of them (Contopus virens and Setophaga striata) showing moderate sensitivity to disturbance. Overall, this demonstrates that agroecosystems can be a part of the habitat used by species in need of global conservation (Díaz-Bohórquez et al., 2014).

CONCLUSIONS

The type II agroecosystem habitats are apparently not completely negative on avifauna. In these agroecosystems, we registered several species that inhabit forests of different regions of the department of Caldas. Therefore, it can be suggested that this type of agroecosystems could play an important role within bird conservation strategies in rural landscapes, where native forests are still conserved. Given this, agroecosystems could be an important element in stewardship planning of areas surrounding natural reserves, since these would cause fewer negative impacts on bird diversity in departments with areas destined for biodiversity conservation, such as Caldas. The conservation strategies in this region should involve farmers, government entities, non-governmental organizations and the general public.

Acknowledgements

ACKNOWLEDGMENTS

This project was funded by COLCIENCIAS (code: 112765740609, contract 684 of 2014) and Vicerrectoría de Investigaciones y Postgrados - Universidad de Caldas (code: 0627416). In addition, this project received support from the Grupo de Investigación en Ecosistemas Tropicales, Grupo de investigación en Genética, Biodiversidad y Manejo de Ecosistemas “GEBIOME” and Grupo de investigación BIOSALUD of the Universidad de Caldas. We thank the institutions and landowners who allowed us to access their properties during field work, among these, Aguas de Manizales S.A E.S.P., Central Hidroeléctrica de Caldas S.A E.S.P, Reserva Forestal de la Sociedad Civil La Gaviota, SMURFIT KAPPA Cartón de Colombia S.A, Sistema Granjas de la Universidad de Caldas. This research was developed under the Framework Agreement for Collection of Specimens of Wild Species of the Biological Diversity with non-commercial scientific research purposes (ANLA Resolution No. 1166).

REFERENCES

  1. Arango N, Armenteras D, Castro M, Gottsmann T, Hernández OL, Matallana CL, Morales M, Naranjo LG, Renjifo LM, Trujillo AF y Villarreal HF. 2003. Vacíos de conservación del Sistema de Parques Nacionales de Colombia desde una perspectiva ecorregional. Primera edición. Editorial Sepia Ltda, Bogotá. 64 p. 🠔
  2. Barlow J, Mestre LAM, Gardner TA and Peres CA. 2007. The value of primary, secondary and plantation forests for Amazonian birds. Biological Conservation 136(2): 212-231. doi: 10.1016/j.biocon.2006.11.021 [DOI] 🠔
  3. Bellocq MI, Filloy J, Zurita GA and Apellaniz MF. 2011. Responses in the abundance of generalist birds to environmental gradients: The rufous-collared sparrow (Zonotrichia capensis) in the southern Neotropics. Ecoscience 18(4): 354-362. doi: 10.2980/18-4-3431 [DOI] 🠔
  4. Blake JG and Loiselle BA. 2001. Bird assemblages in second-growth and old-growth forest, Costa Rica: Perspectives from mist nets and point counts. The Auk 118(2): 304-326. doi: 10.2307/4089793 [DOI] 🠔
  5. Bruinsma J. 2003. World Agriculture: towards 2015/2030 an FAO perspective. Food and Agriculture Organization (FAO). Earthscan Publications Ltd., London. 44 p. 🠔
  6. Castaño-Villa GJ, Morales-Betancourt JA y Bedoya-Álvarez ML. 2008. Aporte de una plantación forestal mixta a la conservación de la avifauna en el Cañon del río Cauca, Colombia. Revista Facultad Nacional de Agronomía Medellín 61(1): 4358-4365. doi: 10.15446/rfnam [DOI] 🠔
  7. Castaño-Villa GJ, Estévez JV and Fontúrbel FE. 2014. The role of native forest plantations in the conservation of neotropical birds: the case of the Andean alder. Journal for Nature Conservation 22(6): 547-551. doi: 10.1016/j.jnc.2014.08.010 [DOI] 🠔
  8. Cárdenas G, Harvey CA, Ibrahim M y Finegan B. 2003. Diversidad y riqueza de aves en diferentes hábitats en un paisaje fragmentado en Cañas, Costa Rica. Agroforestería en las Américas 10(39): 5-8. 🠔
  9. Chazdon RL, Perez CA, Dent D, Sheil D, Lugo AE, Lamb D, Stork NE and Miller SE. 2009. The potential for species conservation in tropical secondary forests. Conservation Biology 23(6): 1406-1417. doi: 10.1111/J.1523-1739.2009.01338.X [DOI] 🠔
  10. Clarke KR. 1993. Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18(1): 117-143. doi: 10.1111/j.1442-9993.1993.tb00438.x [DOI] 🠔
  11. Colwell RK. 2013. EstimateS: Statistical stimation of species richness and shared species from samples. Version 9.1.0. Published at: http://purl.oclc.org/estimates [URL] 🠔
  12. Corporación Autónoma Regional de Caldas (Corpocaldas) y Asociación Calidris. 2010. Estado de conocimiento de las aves en el departamento de Caldas: Prioridades de conservación y vacíos de información. Corpocaldas, Manizales. 105 p. 🠔
  13. Corporación Autónoma Regional de Caldas (Corpocaldas). 2016. Plan de acción institucional 2016-2019. Actualización ambiental del diagnóstico ambiental de Caldas. Corpocaldas, Manizales . 77 p. 🠔
  14. Dent DH and Wright J. 2009. The future of tropical species in secondary forests: A quantitative review. Biological Conservation 142(12): 2833-2843. doi: 10.1016/j.biocon.2009.05.035 [DOI] 🠔
  15. Díaz S, Fargione J, Chapin III FS and Tilman D. 2006. Biodiversity Loss threatens human well-being. PloS Biology 4(8): e277. doi: 10.1371/journal.pbio.0040277 [DOI] 🠔
  16. Faria D, Laps RR, Baumgarten J and Cetra M. 2006. Bat and bird assemblages from forests and shade cacao plantations in two contrasting landscapes in the Atlantic forest of Southern Bahia, Brazil. Biodiversity and Conservation 15(2): 587-612. doi: 10.1007/s10531-005-2089-1 [DOI] 🠔
  17. Fontúrbel FE, Candia AB and Castaño-Villa GJ. 2016. Are abandoned eucalyptus plantations avifauna-friendly? A case study in the Valdivian rainforest. Revista Mexicana de Biodiversidad 87(4): 1402-1406. doi: 10.1016/j.rmb.2016.09.011 [DOI] 🠔
  18. Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA and Sodhi N. 2009. Prospects for tropical forest biodiversity in a human-modified world. Ecology Letters 12(6): 561-582. doi: 10.1111/j.1461-0248.2009.01294.x [DOI] 🠔
  19. Greenberg R, Bichier P and Sterling J. 1997. Bird populations in rustic and planted shade coffee plantations of eastern Chiapas, Mexico. Biotropica 29(4): 501-514. doi: 10.1111/j.1744-7429.1997.tb00044.x [DOI] 🠔
  20. Gentry A. 1992. Tropical forest biodiversity: Distributional patterns and their conservational significance. Oikos 63(1): 19-28. doi: 10.2307/3545512 [DOI] 🠔
  21. Gibson L, Ming Lee T, Pin Koh L, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJA, Laurance WF, Lovejoy TE and Sodhi NS. 2011. Primary forests are irreplaceable for sustaining tropical biodiversity Nature 478(7369): 378-381. doi: 10.1038/nature10425 [DOI] 🠔
  22. Hammer Ø, Harper DAT and Ryan PD. 2001. PAST: Paleontological statistic software package for education and data analysis. Palaeontologia Electronica 4(1): 1-9. 🠔
  23. Hanula JL, Horn S and O'Brien JJ. 2015. Have changing forests conditions contributed to pollinator decline in the southeastern United States? Forest Ecology and Management 348: 142-152. doi: 10.1016/j.foreco.2015.03.044 [DOI] 🠔
  24. International Union for Conservation of Nature. 2016. The IUCN Red List of threatened species. Version 2016-3. In: In: www.iucnredlist.org . 2307-8235. Accessed: March 2017. [URL] 🠔
  25. Jaramillo-Robledo A, Ramírez-Builes VH, y Arcila-Pulgarín J. 2011. Patrones de distribución de la lluvia en la zona cafetera. Programa de Investigación Científica Fondo Nacional del Café. Cenicafé, Chinchiná. 12 p. 🠔
  26. Lozano-Zambrano FH, Mendoza-Sabogal JE, Vargas-Franco AM, Renjifo LM, Jiménez E, Caycedo PC, Vargas W, Aristizábal SL y Ramírez DP. 2009. Capítulo 3: Oportunidades de conservación en el paisaje rural. pp. 41-80. En: Lozano-Zambrano FH (ed). 2009. Herramientas de manejo para la conservación de biodiversidad en paisajes rurales. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt y Corporación Autónoma Regional de Cundinamarca (CAR), Bogotá, D. C. 238 p. 🠔
  27. MacGregor-Fors I and Payton ME. 2013. Contrasting diversity values: Statistical Inferences based on overlapping confidence intervals. Plos One 8(2): e56794. doi: 10.1371/journal.pone.0056794 [DOI] 🠔
  28. Ministerio de Agricultura y Desarrollo Rural-MADR., Gobernación de Caldas, Fondo Nacional de Fomento Hortifrutícola-FNFH, Asociación Hortifrutícola de Colombia-Asohofrucol y Sociedad de Agricultores y Ganaderos del Valle del Cauca SAG. 2006. Plan Frutícola Nacional, desarrollo de la fruticultura en Caldas. Manizales. 80 p. 🠔
  29. Nájera A and JA Simonetti. 2010. Enhancing avifauna in comercial plantations. Conservation Biology 24(1): 319-324. doi: 10.1111/j.1523-1739.2009.01350.x [DOI] 🠔
  30. Pejchar L, Pringle R, Ranganathana J, Zook JR, Duran G, Oviedo F and Daily GC. 2008. Birds as agents of seed dispersal in a human-dominated landscape in southern Costa Rica. Biological Conservation 141(2): 536-544. doi: 10.1016/j.biocon.2007.11.008 [DOI] 🠔
  31. Petit LJ, Petit DR, Christian DG and Powell HDW. 1999. Bird communities of natural and modified habitats in Panama. 1999. Ecography 22(3): 292-304. doi: 10.1111/j.1600-0587.1999.tb00505.x [DOI] 🠔
  32. Petit LJ and Petit DR . 2003. Evaluating the importance of human-modified lands for neotropical bird conservation. Conservation Biology 17(3): 687-694. doi: 10.1046/j.1523-1739.2003.00124.x [DOI] 🠔
  33. Philpott SM and Bichier P. 2012. Effects of shade tree removal on birds in coffee agroecosystems in Chiapas, Mexico. Agriculture, Ecosystems and Environment 149(1): 171-180. doi: 10.1016/j.agee.2011.02.015 [DOI] 🠔
  34. R Development Core Team. 2017. R: a Language and enviroment for statistical computing, reference index Version 3.4.3. Foundation for Statistical Computing, Vienna, Austria. 🠔
  35. Remsen JV, Cadena CD, Jaramillo A, Nores M, Pacheco JF, Perez-Eman J, Robbins MB, Stiles FG, Stotz DF and Zimmer KJ. 2017. Version 22-April-2017. A classification of the bird species of South America. American Ornithologists' Union. 🠔
  36. Restall R, Rodner C and Lentino M. 2007. Birds of Northern South America. An identification guide. Volume 1. Yale University Press. 880 p. 🠔
  37. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber E, Huenneke LF, Jackson R, Kinzig A, Lodge D, Oesterheld M, Poff NL, Sykes M, Walker B, Walker M and Wall DH. 2000. Global biodiversity scenarios for the year 2100. Science 287(5459): 1770-1774. doi: 10.1126/science.287.5459.1770 [DOI] 🠔
  38. Simonetti JA, Grez AA and Estades CF. 2012. Biodiversity conservation in agroforestry landscapes. First edition. Editorial Universitaria S.A, Santiago de Chile. 162 p. 🠔
  39. Stotz DF, Fitzpatrick JW, Parker III TA and Moskovist DK. 1996. Neotropical birds: Ecology and conservation. First edition. University of Chicago Pr, Chicago. 502 p. 🠔
  40. Vergara-Paternima JA, Ballesteros-Correo J, González charrasquiel C y Linares-Arias JC. 2017. Diversidad de aves en fragmentos de bosque seco tropical en paisajes ganaderos del Departamento de Córdoba, Colombia. Revista de Biología Tropical 65(4): 1625-1634. doi: 10.15517/rbt.v65i4.26313 [DOI] 🠔
  41. Wood S, Sebastian K and Scherr SJ. 2000. Pilot analysis of global ecosystems. International Food Policy Research Institute and World Resources Institute, Washington, DC, 111 p. 🠔