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Biological corridors as important habitat structures for maintaining bees in a tropical fragmented landscape

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Abstract

Biological corridors are an important conservation strategy to increase connectivity between populations—mainly vertebrates—in fragmented landscapes, which often require habitat restoration to achieve physical connections. Non-target groups such as bees could benefit from corridors while contributing to the restoration process given their role as pollinators, but little is known about the use of corridors by bees. Here we assessed the habitat value for bees of four biological corridors in the Colombian Andes by comparing bee species richness, community composition and functional diversity between corridors (which had two land-cover sections: riparian forest and restored forest), forest patches being connected by corridors and surrounding pastures. We found a higher species richness in riparian than in restored sections of corridors, which was comparable to that in forest and higher than in pasture. Community composition in forest and riparian sections were similar and differed from that in pasture. In contrast, functional diversity was similar among all land-use types, suggesting a higher species redundancy in forest and riparian corridors, given the higher species richness, compared to pastures. Our results show that riparian corridors are holding forest-associated species that could not survive in pastures, and given the higher redundancy, can significantly contribute to the maintenance of pollination services in fragmented landscapes. Our results also indicate that 13 years of restoration process have not been sufficient to reach reference levels (i.e. forest/riparian) in terms of bee species richness, but the recovery of some forest-associated species points to the potential of biological corridors to functionally connect forest patches.

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References

  1. Araújo ED, Costa M, Chaud-Netto J, Fowler HG (2004) Body size and flight distance in stingless bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implications. Braz J Biol 64:563–568

  2. Audino LD, Louzada J, Comita L (2014) Dung beetles as indicators of tropical forest restoration success: is it possible to recover species and functional diversity? Biol Conserv 169:248–257

  3. Basu P, Parui AK, Chatterjee S, Dutta A, Chakraborty P, Roberts S, Smith B (2016) Scale dependent drivers of wild bee diversity in tropical heterogeneous agricultural landscapes. Ecol Evol 6:6983–6992

  4. Beier P, Noss RF (1998) Do habitat corridors provide connectivity? Conserv Biol 12:1241–1252

  5. Bennett AF (1999) Linkages in the landscape: the role of corridors and connectivity in wildlife conservation. IUCN Publications Services Unit, UK

  6. Bommarco R, Biesmeijer JC, Meyer B, Potts SG, Pöyry J, Roberts SP, Steffan-Dewenter I, Öckinger E (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc R Soc B 277:2075–2082

  7. Brosi BJ (2009a) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biol Conserv 142:414–423

  8. Brosi BJ (2009b) The complex responses of social stingless bees (Apidae: Meliponini) to tropical deforestation. For Ecol Manag 258:1830–1837

  9. Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2008) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45:773–783

  10. Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087

  11. Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kansas Entomol Soc 60:145–147

  12. Carmona CP, de Bello F, Mason NW, Lepš J (2016) Traits without borders: integrating functional diversity across scales. Trends Ecol Evol 31:382–394

  13. Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547

  14. Cisneros LM, Fagan ME, Willig MR (2015) Effects of human-modified landscapes on taxonomic, functional and phylogenetic dimensions of bat biodiversity. Divers Distrib 21:523–533

  15. Clarke KR, Gorley RN (2006) User manual/tutorial. Primer-E Ltd., Plymouth, p 93

  16. Cracco M, Guerrero E (2004) Aplicación del Enfoque Ecosistemático a la gestión de corredores en América del Sur. Memorias del Taller Regional, 3 al 5 de junio. UICN, Quito, Ecuador

  17. Cranmer L, McCollin D, Ollerton J (2012) Landscape structure influences pollinator movements and directly affects plant reproductive success. Oikos 121:562–568

  18. Crooks KR, Sanjayan M (2006) Connectivity conservation. Cambridge University Press, Cambridge

  19. Cuatrecasas J (1958) Aspectos de la vegetación natural en Colombia. Revista Acadademia Colombiana Ciencias Exactas, Fisicas y Naturales 10:221–268

  20. De Arruda Almeida B, Green AJ, Sebastián-González E, dos Anjos L (2018) Comparing species richness, functional diversity and functional composition of waterbird communities along environmental gradients in the Neotropics. PLoS ONE 13:e0200959

  21. Dı́az S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655

  22. Etter A, McAlpine C, Pullar D, Possingham H (2006) Modelling the conversion of Colombian lowland ecosystems since 1940: drivers, patterns and rates. J Environ Manag 79:74–87

  23. Fagua JC, Cabrera E, Gonzalez VH (2013) The effect of highly variable topography on the spatial distribution of Aniba perutilis (Lauraceae) in the Colombian Andes. Revista de Biología Tropical 61:301–309

  24. Forrest JR, Thorp RW, Kremen C, Williams NM (2015) Contrasting patterns in species and functional-trait diversity of bees in an agricultural landscape. J Appl Ecol 52:706–715

  25. Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhöffer JH, Greenleaf SS et al (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072

  26. Gonzalez VH, Griswold T, Engel MS (2013) Obtaining a better taxonomic understanding of native bees: where do we start? Syst Entomol 38:645–653

  27. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

  28. Gotelli NJ, Colwell RK (2010) Estimating species richness Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford

  29. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

  30. Gutiérrez-Chacón C, Franco P, Solano C (2013) Iniciativas de conectividad en Colombia, in: In: Hurtado A., Santamaría M. y Matallana-Tobón C.L. Plan de Investigación y Monitoreo Del Sistema Nacional de Áreas Protegidas (Sinap): Avances Construidos Desde La Mesa de Investigación y Monitoreo Entre 2009 y 2012. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt y Parques Nacionales Naturales, Bogotá D.C, Colombia, p 200

  31. Gutiérrez-Chacón C, Dormann CF, Klein A-M (2018) Forest-edge associated bees benefit from the proportion of tropical forest regardless of its edge length. Biol Conserv 220:149–160

  32. Herrera-Rangel J, Jiménez-Carmona E, Armbrecht I (2015) Monitoring the diversity of hunting ants (Hymenoptera: Formicidae) on a fragmented and restored andean landscape. Environ Entomol 44:1287–1298

  33. Hill CJ (1995) Linear strips of rain forest vegetation as potential dispersal corridors for rain forest insects. Conserv Biol 9:1559–1566

  34. Hilty JA, Lidicker WZ Jr, Merenlender A (2012) Corridor ecology: the science and practice of linking landscapes for biodiversity conservation. Island Press, Washington DC

  35. Hsieh TC, Ma KH, Chao A (2016) iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.12. https://chao.shinyapps.io/iNEXTOnline/. Accessed 1 Dec 2019

  36. Hunter MD (2002) Landscape structure, habitat fragmentation, and the ecology of insects. Agric For Entomol 4:159–166

  37. Jauker B, Krauss J, Jauker F, Steffan-Dewenter I (2013) Linking life history traits to pollinator loss in fragmented calcareous grasslands. Landsc Ecol 28:107–120

  38. Kaluza BF, Wallace HM, Heard TA, Minden V, Klein A, Leonhardt SD (2018) Social bees are fitter in more biodiverse environments. Sci Rep 8:12353

  39. Kattan GH, Franco P, Rojas V, Morales G (2004) Biological diversification in a complex region: a spatial analysis of faunistic diversity and biogeography of the Andes of Colombia. J Biogeogr 31:1829–1839

  40. Kremen C, Chaplin-Kramer R (2007) Insects as providers of ecosystem services: crop pollination and pest control, in: Insect Conservation Biology. In: Proceedings of the Royal Entomological Society’s 23rd Symposium. pp 349–382

  41. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305

  42. Lichtenberg EM, Mendenhall CD, Brosi B (2017) Foraging traits modulate stingless bee community disassembly under forest loss. J Anim Ecol 86:1404–1416

  43. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323

  44. Lozano-Zambrano FH (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)

  45. Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton

  46. Mendoza JE, Lozano FH (2006) Composición y estructura de la biodiversidad en paisajes transformados en Colombia (1998-2005). In: Chaves ME, Santamaría M (eds) Informe sobre el avance en el conocimiento y la formación de la biodiversidad 1998-2004. Bogotá, Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, pp 67–84

  47. Michener CD (2007) The bees of the world. Johns Hopkins University Press, Baltimore, p 953

  48. Nemésio A (2012) Methodological concerns and challenges in ecological studies with orchid bees (Hymenoptera: Apidae: Euglossina). Biosci J 28(1):118–135

  49. Ngo HT, Gibbs J, Griswold T, Packer L (2013) Evaluating bee (Hymenoptera: Apoidea) diversity using Malaise traps in coffee landscapes of Costa Rica. Can Entomol 145:435–453

  50. Nieh J (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182

  51. Nuttman CV, Otieno M, Kwapong PK, Combey R, Willmer P, Potts SG (2011) The utility of aerial pan-trapping for assessing insect pollinators across vertical strata. J Kansas Entomol Soc 84:260–270

  52. Öckinger E, Smith HG (2008) Do corridors promote dispersal in grassland butterflies and other insects? Landsc Ecol 23:27–40

  53. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

  54. Park MG, Blitzer EJ, Gibbs J, Losey JE, Danforth BN (2015) Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proc R Soc B 282(1809):20150299

  55. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758

  56. Rader R, Bartomeus I, Tylianakis JM, Laliberté E (2014) The winners and losers of land use intensification: pollinator community disassembly is non-random and alters functional diversity. Divers Distrib 20:908–917

  57. Roubik DW (1992) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge

  58. Roubik DW (1995) Pollination of cultivated plants in the tropics. Food & Agriculture Org

  59. Rudnick D, Ryan SJ, Beier P, Cushman SA, Dieffenbach F, Epps C, Gerber LR, Hartter J, Jenness JS, Kintsch J et al (2012) The role of landscape connectivity in planning and implementing conservation and restoration priorities. Issues in Ecology

  60. Ryan R, Harper DA, Whalley JS (1994) PALSTAT: user’s manual and case histories: statistics for palaeontologists and palaeobiologists. Springer, New York

  61. Steffan-Dewenter I (2002) Landscape context affects trap-nesting bees, wasps, and their natural enemies. Ecol Entomol 27:631–637

  62. Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Clough Y, Crist TO, Dormann CF et al (2012) Landscape moderation of biodiversity patterns and processes-eight hypotheses. Biol Rev 87:661–685

  63. Vargas WG (2008) Evaluación de dos estrategias de restauración, su aplicación y evaluación en el establecimiento del corredor Barbas-Bremen, Quindío. Universidad del valle, Programa biología, Maestría en ciencias. Tesis, Santiago de Cali

  64. Vélez D, Pulido-Barrios H (2005) Observations on the vertical stratification of orchid bees (Apidae: Euglossini) in a riparian forest of the Colombian Orinoquia. Caldasia 2:267–270

  65. Viana BF, Boscolo D, Neto EM, Lopes LE, Lopes AV, Ferreira PA, Pigozzo C, Primo L (2012) How well do we understand landscape effects on pollinators and pollination services? J Pollinat Ecol 7:31–41

  66. Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

  67. Williams NM (2011) Restoration of nontarget species: bee communities and pollination function in riparian forests. Restor Ecol 19:450–459

  68. Williams NM, Crone EE, Minckley RL, Packer L, Potts SG et al (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291

  69. Winfree R, Griswold T, Kremen C (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21:213–223

  70. Winsa M, Öckinger E, Bommarco R, Lindborg R, Roberts SP, Wärnsberg J, Bartomeus I (2017) Sustained functional composition of pollinators in restored pastures despite slow functional restoration of plants. Ecol Evol 7:3836–3846

  71. Wortley L, Hero J-M, Howes M (2013) Evaluating ecological restoration success: a review of the literature. Restor Ecol 21:537–543

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Acknowledgements

We thank J.C. Mejía, M.B. Duque, F. Builes, J. Builes, H.F. Gómez, H. Castro, S. Giraldo, and landowners in Filandia for research permission and valuable help with fieldwork. We further thank our field assistants, M. Rodriguez, J. Home, L.F. Estrada and F. Gamboa, V.H González and R. Ospina for their help with bee identification, and C. Ríos for GIS help. We would like to thank CRQ (Corporación Autónoma Regional del Quindío) for the research permit No. 576-2014 and Universidad del Valle for research facilities; C.G.C was funded by COLCIENCIAS (Colombian Administrative Department of Science, Technology and Innovation). This study was also supported by the University of Freiburg, Universidad Icesi, the Colombian Biodiversity Research Institute Alexander von Humboldt and Wildlife Conservation Society (WCS).

Funding

Corresponding author Catalina Gutiérrez-Chacón received financial support from the Colombian Administrative Department of Science, Technology and Innovation (COLCIENCIAS), through a doctorate scholarship (No. 049). Field work for this study was supported by the Colombian Biodiversity Research Institute Alexander von Humboldt, Universidad Icesi and Wildlife Conservation Society (WCS)—Colombia Program.

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Correspondence to Catalina Gutiérrez-Chacón.

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Gutiérrez-Chacón, C., Valderrama-A, C. & Klein, A. Biological corridors as important habitat structures for maintaining bees in a tropical fragmented landscape. J Insect Conserv (2019). https://doi.org/10.1007/s10841-019-00205-2

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Keywords

  • Restoration
  • Species traits
  • Tropical forest
  • Connectivity
  • Colombia