Table of Contents
Advances in Ecology
Volume 2014 (2014), Article ID 379267, 7 pages
http://dx.doi.org/10.1155/2014/379267
Review Article

Microevolutionary Effects of Habitat Fragmentation on Plant-Animal Interactions

Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Ñuñoa, 7800024 Santiago, Chile

Received 26 May 2014; Revised 4 August 2014; Accepted 8 August 2014; Published 25 August 2014

Academic Editor: Tomasz S. Osiejuk

Copyright © 2014 Francisco E. Fontúrbel and Maureen M. Murúa. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. R. Darwin, On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, John Murray, London, UK, 1859.
  2. C. R. Darwin, On the Various Contrivances by Which British and Foreign Orchids are Fertilised by Insects, John Murray, London, UK, 1862.
  3. A. Pauw, J. Stofberg, and R. J. Waterman, “Flies and flowers in Darwin's race,” Evolution, vol. 63, no. 1, pp. 268–279, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. D. H. Janzen, “When it is coevolution?” Evolution, vol. 34, no. 3, pp. 611–612, 1980. View at Google Scholar
  5. P. R. Ehrlich and P. H. Raven, “Butterflies and plants: a study in coevolution,” Evolution, vol. 18, no. 4, pp. 586–608, 1964. View at Google Scholar
  6. M. A. Rodríguez-Cabal, M. A. Aizen, and A. J. Novaro, “Habitat fragmentation disrupts a plant-disperser mutualism in the temperate forest of South America,” Biological Conservation, vol. 139, no. 1-2, pp. 195–202, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. E. T. Kiers, T. M. Palmer, A. R. Ives, J. F. Bruno, and J. L. Bronstein, “Mutualisms in a changing world: an evolutionary perspective,” Ecology Letters, vol. 13, no. 12, pp. 1459–1474, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. P. L. González-Gómez, C. F. Estades, and J. A. Simonetti, “Strengthened insectivory in a temperate fragmented forest,” Oecologia, vol. 148, no. 1, pp. 137–143, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. J. P. Arnold and C. R. Fonseca, “Herbivory, pathogens, and epiphylls in araucaria forest and ecologically-managed tree monocultures,” Forest Ecology and Management, vol. 262, no. 6, pp. 1041–1046, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Groppe, T. Steinger, B. Schmid, B. Baur, and T. Boller, “Effects of habitat fragmentation on choke disease (Epichloë bromicola) in the grass Bromus erectus,” Journal of Ecology, vol. 89, no. 2, pp. 247–255, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. K. McGarigal and S. A. Cushman, “Comparative evaluation of experimental approaches to the study of habitat fragmentation effects,” Ecological Applications, vol. 12, no. 2, pp. 335–345, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. P. H. Thrall, M. E. Hochberg, J. J. Burdon, and J. D. Bever, “Coevolution of symbiotic mutualists and parasites in a community context,” Trends in Ecology and Evolution, vol. 22, no. 3, pp. 120–126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Fahrig, “Relative effects of habitat loss and fragmentation on population extinction,” Journal of Wildlife Management, vol. 61, no. 3, pp. 603–610, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. R. M. Ewers and R. K. Didham, “Confounding factors in the detection of species responses to habitat fragmentation,” Biological Reviews of the Cambridge Philosophical Society, vol. 81, no. 1, pp. 117–142, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. L. F. Keller and D. M. Waller, “Inbreeding effects in wild populations,” Trends in Ecology and Evolution, vol. 17, no. 5, pp. 230–241, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. M. L. Lancaster, A. C. Taylor, S. J. B. Cooper, and S. M. Carthew, “Limited ecological connectivity of an arboreal marsupial across a forest/plantation landscape despite apparent resilience to fragmentation,” Molecular Ecology, vol. 20, no. 11, pp. 2258–2271, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Andrén, “Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review,” Oikos, vol. 71, no. 3, pp. 355–366, 1994. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Fahrig, “Effects of habitat fragmentation on biodiversity,” Annual Review of Ecology, Evolution, and Systematics, vol. 34, pp. 487–515, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. J. M. Herrera, J. M. Morales, and D. García, “Differential effects of fruit availability and habitat cover for frugivore-mediated seed dispersal in a heterogeneous landscape,” Journal of Ecology, vol. 99, no. 5, pp. 1100–1107, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Bowman, C. Perret, S. Hoehn, D. J. Galeuchet, and M. Fischer, “Habitat fragmentation and adaptation: a reciprocal replant-transplant experiment among 15 populations of Lychnis flos-cuculi,” Journal of Ecology, vol. 96, no. 5, pp. 1056–1064, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. N. G. Hairston Jr., S. P. Ellner, M. A. Geber, T. Yoshida, and J. A. Fox, “Rapid evolution and the convergence of ecological and evolutionary time,” Ecology Letters, vol. 8, no. 10, pp. 1114–1127, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Murúa, C. Espinoza, R. Bustamante, V. H. Marín, and R. Medel, “Does human-induced habitat transformation modify pollinator-mediated selection? A case study in Viola portalesia (Violaceae),” Oecologia, vol. 163, no. 1, pp. 153–162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Tobler and I. Schlupp, “Expanding the horizon: the Red Queen and potential alternatives,” Canadian Journal of Zoology, vol. 86, no. 8, pp. 765–773, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. M. T. Kinnison and N. G. Hairston Jr., “Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence,” Functional Ecology, vol. 21, no. 3, pp. 444–454, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. T. Kinnison, A. P. Hendry, and C. A. Stockwell, “Contemporary evolution meets conservation biology II: impediments to integration and application,” Ecological Research, vol. 22, no. 6, pp. 947–954, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. C. A. Stockwell, A. P. Hendry, and M. T. Kinnison, “Contemporary evolution meets conservation biology,” Trends in Ecology and Evolution, vol. 18, no. 2, pp. 94–101, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Galetti, R. Guevara, M. C. Côrtes et al., “Functional extinction of birds drives rapid evolutionary changes in seed size,” Science, vol. 340, no. 6136, pp. 1086–1090, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. E. M. Albert, M. A. Fortuna, J. A. Godoy, and J. Bascompte, “Assessing the robustness of networks of spatial genetic variation,” Ecology Letters, vol. 16, no. 1, pp. 86–93, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Bascompte and P. Jordano, “Plant-animal mutualistic networks: the architecture of biodiversity,” Annual Review of Ecology, Evolution, and Systematics, vol. 38, pp. 567–593, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Ashworth, R. Aguilar, L. Galetto, and M. A. Aizen, “Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation?” Journal of Ecology, vol. 92, no. 4, pp. 717–719, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. J. N. Thompson, “Specific hypotheses on the geographic mosaic of coevolution,” American Naturalist, vol. 153, no. S5, pp. S1–S14, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Sachs and E. L. Simms, “Pathways to mutualism breakdown,” Trends in Ecology and Evolution, vol. 21, no. 10, pp. 585–592, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Gascon, T. E. Lovejoy, R. O. Bierregaard Jr. et al., “Matrix habitat and species richness in tropical forest remnants,” Biological Conservation, vol. 91, no. 2-3, pp. 223–229, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Tscharntke and R. Brandl, “Plant-insect interactions in fragmented landscapes,” Annual Review of Entomology, vol. 49, no. 1, pp. 405–430, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Barlow, C. A. Peres, L. M. P. Henriques, P. C. Stouffer, and J. M. Wunderle, “The responses of understorey birds to forest fragmentation, logging and wildfires: an Amazonian synthesis,” Biological Conservation, vol. 128, no. 2, pp. 182–192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. D. A. Kelt, “Differential effects of habitat fragmentation on birds and mammals in Valdivian temperate rainforests,” Revista Chilena de Historia Natural, vol. 74, no. 4, pp. 769–777, 2001. View at Google Scholar
  37. R. Pardini, S. M. De Souza, R. Braga-Neto, and J. P. Metzger, “The role of forest structure, fragment size and corridors in maintaining small mammal abundance and diversity in an Atlantic forest landscape,” Biological Conservation, vol. 124, no. 2, pp. 253–266, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. R. K. Didham, J. Ghazoul, N. E. Stork, and A. J. Davis, “Insects in fragmented forests: a functional approach,” Trends in Ecology and Evolution, vol. 11, no. 6, pp. 255–260, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. A. . Grez, T. Zaviezo, L. Tischendorf, and L. Fahrig, “A transient, positive effect of habitat fragmentation on insect population densities,” Oecologia, vol. 141, no. 3, pp. 444–451, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. A. E. Arnold and N. M. Asquith, “Herbivory in a fragmented tropical forest: patterns from islands at Lago Gatún, Panama,” Biodiversity and Conservation, vol. 11, no. 9, pp. 1663–1680, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. P. A. Vásquez, A. A. Grez, R. O. Bustamante, and J. A. Simonetti, “Herbivory, foliar survival and shoot growth in fragmented populations of Aristotelia chilensis,” Acta Oecologica, vol. 31, no. 1, pp. 48–53, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. D. S. Donoso, A. A. Grez, and J. A. Simonetti, “Effects of forest fragmentation on the granivory of differently sized seeds,” Biological Conservation, vol. 115, no. 1, pp. 63–70, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Aguilar, L. Ashworth, L. Galetto, and M. A. Aizen, “Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis,” Ecology Letters, vol. 9, no. 8, pp. 968–980, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. M. A. Aizen and P. Feinsinger, “Forest fragmentation, pollination, and plant reproduction in a chaco dry forest, Argentina,” Ecology, vol. 75, no. 2, pp. 330–351, 1994. View at Publisher · View at Google Scholar · View at Scopus
  45. N. J. Cordeiro and H. F. Howe, “Low recruitment of trees dispersed by animals in African forest fragments,” Conservation Biology, vol. 15, no. 6, pp. 1733–1741, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. J. N. Thompson, The Coevolutionary Process, The Chicago University Press, Chicago, Ill, USA, 1994.
  47. F. Howe and J. Smallwood, “Ecology of seed dispersal.,” Annual review of ecology and systematics. Volume 13, pp. 201–228, 1982. View at Google Scholar · View at Scopus
  48. J. Ollerton, A. Stott, E. Allnutt, S. Shove, C. Taylor, and E. Lamborn, “Pollination niche overlap between a parasitic plant and its host,” Oecologia, vol. 151, no. 3, pp. 473–485, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. B. L. Johnson and N. M. Haddad, “Edge effects, not connectivity, determine the incidence and development of a foliar fungal plant disease,” Ecology, vol. 92, no. 8, pp. 1551–1558, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Valladares, A. Salvo, and L. Cagnolo, “Habitat fragmentation effects on trophic processes of insect-plant food webs,” Conservation Biology, vol. 20, no. 1, pp. 212–217, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. D. M. Evans, N. E. Turley, and J. J. Tewksbury, “Habitat edge effects alter ant-guard protection against herbivory,” Landscape Ecology, vol. 28, no. 9, pp. 1743–1754, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. L. L. Sullivan, B. L. Johnson, L. A. Brudvig, and N. M. Haddad, “Can dispersal mode predict corridor effects on plant parasites?” Ecology, vol. 92, no. 8, pp. 1559–1564, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. A. G. Auffret and J. Plue, “Scale-dependent diversity effects of seed dispersal by a wild herbivore in fragmented grasslands,” Oecologia, vol. 175, no. 1, pp. 305–313, 2014. View at Google Scholar
  54. E. S. Jules and P. Shahani, “A broader ecological context to habitat fragmentation: why matrix habitat is more important than we thought,” Journal of Vegetation Science, vol. 14, no. 3, pp. 459–464, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Kruess and T. Tscharntke, “Habitat fragmentation, species loss, and biological control,” Science, vol. 264, no. 5165, pp. 1581–1584, 1994. View at Publisher · View at Google Scholar · View at Scopus
  56. D. T. Bolger, A. C. Alberts, R. M. Sauvajot et al., “Response of rodents to habitat fragmentation in coastal southern California,” Ecological Applications, vol. 7, no. 2, pp. 552–563, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. T. D. Castellón and K. E. Sieving, “Landscape history, fragmentation, and patch occupancy: models for a forest bird with limited dispersal,” Ecological Applications, vol. 16, no. 6, pp. 2223–2234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. K. R. Crooks, “Relative sensitivities of mammalian carnivores to habitat fragmentation,” Conservation Biology, vol. 16, no. 2, pp. 488–502, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. T. J. Kawecki and D. Ebert, “Conceptual issues in local adaptation,” Ecology Letters, vol. 7, no. 12, pp. 1225–1241, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. C. E. Valdivia, A. Bahamondez, and J. A. Simonetti, “Negative effects of forest fragmentation and proximity to edges on pollination and herbivory of Bomarea salsilla (Alstroemeriaceae),” Plant Ecology and Evolution, vol. 144, no. 3, pp. 281–287, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Pohl, G. Carvallo, C. Botto-Mahan, and R. Medel, “Nonadditive effects of flower damage and hummingbird pollination on the fecundity of Mimulus luteus,” Oecologia, vol. 149, no. 4, pp. 648–655, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. W. S. Armbuster, “Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry,” Ecology, vol. 78, no. 6, pp. 1661–1672, 1997. View at Google Scholar · View at Scopus
  63. C. M. Herrera, “Measuring the effects of pollinators and herbivores: evidence for non-additivity in a perennial herb,” Ecology, vol. 81, no. 8, pp. 2170–2176, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Y. Strauss and R. E. Irwin, “Ecological and evolutionary consequences of multispecies plant-animal interactions,” Annual Review of Ecology, Evolution, and Systematics, vol. 35, pp. 435–466, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Y. Strauss, “Indirect effects in community ecology: their definition, study and importance,” Trends in Ecology and Evolution, vol. 6, no. 7, pp. 206–210, 1991. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Y. Strauss, “Floral characters link herbivores, pollinators, and plant fitness,” Ecology, vol. 78, no. 6, pp. 1640–1645, 1997. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Y. Strauss and W. S. Armbruster, “Linking herbivory and pollination: new perspectives on plant and animal ecology and evolution,” Ecology, vol. 78, no. 6, pp. 1617–1618, 1997. View at Google Scholar · View at Scopus
  68. R. Medel, C. Botto-Mahan, and M. Kalin-Arroyo, “Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus,” Ecology, vol. 84, no. 7, pp. 1721–1732, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. G. A. Krupnick and A. E. Weis, “The effect of floral herbivory on male and female reproductive success in Isomeris arborea,” Ecology, vol. 80, no. 1, pp. 135–149, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. G. A. Krupnick, A. E. Weis, and D. R. Campbell, “The consequences of floral herbivory for pollinator service to Isomeris arborea,” Ecology, vol. 80, no. 1, pp. 125–134, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Lehtilä and S. Y. Strauss, “Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum,” Oecologia, vol. 111, no. 3, pp. 396–403, 1997. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Y. Strauss, J. K. Conner, and S. L. Rush, “Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female plant fitness,” The American Naturalist, vol. 147, no. 6, pp. 1098–1107, 1996. View at Publisher · View at Google Scholar · View at Scopus
  73. O. Barbosa and P. A. Marquet, “Effects of forest fragmentation on the beetle assemblage at the relict forest of Fray Jorge, Chile,” Oecologia, vol. 132, no. 2, pp. 296–306, 2002. View at Publisher · View at Google Scholar · View at Scopus
  74. K. F. Davies and C. R. Margules, “Effects of habitat fragmentation on carabid beetles: experimental evidence,” Journal of Animal Ecology, vol. 67, no. 3, pp. 460–471, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. C. E. Valdivia, J. A. Simonetti, and C. A. Henríquez, “Depressed pollination of Lapageria rosea Ruiz et Pav. (Philesiaceae) in the fragmented temperate rainforest of southern South America,” Biodiversity and Conservation, vol. 15, no. 5, pp. 1845–1856, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. Y. J. Cardel and S. Koptur, “Effects of florivory on the pollination of flowers: an experimental field study with a perennial plant,” International Journal of Plant Sciences, vol. 171, no. 3, pp. 283–292, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. A. C. McCall and R. E. Irwin, “Florivory: the intersection of pollination and herbivory,” Ecology Letters, vol. 9, no. 12, pp. 1351–1365, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. C. Botto-Mahan, P. A. Ramírez, C. G. Ossa, R. Medel, M. Ojeda-Camacho, and A. V. González, “Floral herbivory affects female reproductive success and pollinator visitation in the perennial herb Alstroemeria Ligtu (Alstroemeriaceae),” International Journal of Plant Sciences, vol. 172, no. 9, pp. 1130–1136, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Cares-Suárez, T. Poch, R. F. Acevedo et al., “Do pollinators respond in a dose-dependent manner to flower herbivory? An experimental assessment in Loasa tricolor (Loasaceae),” Gayana: Botanica, vol. 68, no. 2, pp. 176–181, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Leimu, A. Muola, L. Laukkanen, A. Kalske, N. Prill, and P. Mutikainen, “Plant-herbivore coevolution in a changing world,” Entomologia Experimentalis et Applicata, vol. 144, no. 1, pp. 3–13, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. F. Peter, D. G. Berens, and N. Farwig, “Effects of local tree diversity on herbivore communities diminish with increasing forest fragmentation on the landscape scale,” PLoS ONE, vol. 9, no. 4, Article ID e95551, 2014. View at Google Scholar
  82. D. Fox, “Back to the no-analog future?” Science, vol. 316, no. 5826, pp. 823–825, 2007. View at Publisher · View at Google Scholar · View at Scopus