Plant-animal interactions are a key component for biodiversity maintenance, but they are currently threatened by human activities. Habitat fragmentation might alter ecological interactions due to demographic changes, spatial discontinuities, and edge effects. Also, there are less evident effects of habitat fragmentation that potentially alter selective forces and compromise the fitness of the interacting species. Changes in the mutualistic and antagonistic interactions in fragmented habitats could significantly influence the plant reproductive output and the fauna assemblage associated with. Fragmented habitats may trigger contemporary evolution processes and open new evolutionary opportunities. Interacting parties with a diffuse and asymmetric relationship are less susceptible to local extinction but more prone to evolve towards new interactions or autonomy. However, highly specialized mutualisms are likely to disappear. On the other hand, ecological interactions may mutually modulate their response in fragmented habitats, especially when antagonistic interactions disrupt mutualistic ones. Ecoevolutionary issues of habitat fragmentation have been little explored, but the empiric evidence available suggests that the complex modification of ecological interactions in fragmented habitats might lead to nonanalogous communities on the long term. 1. Introduction Plant-animal coevolution was described for the first time by Darwin ([1, 2], but see [3]), relating the morphologic specificity between orchids and moths, stating that such precise correspondence could not be generated by chance. From Darwin’s ideas, a wide conceptual framework has been developed regarding plant-animal coevolution [4, 5], from the perspective of the antagonistic (herbivory and parasitism) and mutualistic (pollination and seed dispersal) interactions. There is a growing body of literature regarding the importance of plant-animal interactions for the ecosystem functionality and stability. Moreover, those interactions are not constant over time; on the contrary, they are highly dynamic and susceptible to small and large temporal (ecological and geological times, resp.) and spatial (patch and landscape, resp.) scale disturbances. In the last decades, human activities have led to habitat loss and fragmentation worldwide, causing the disruption of plant-animal mutualisms [6, 7] and the strengthening of some antagonisms [8–10]. While, in the last 15 years, the ecological consequences of habitat fragmentation have been studied in detail [11] but the microevolutionary aspects related to the
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.
[4]
D. H. Janzen, “When it is coevolution?” Evolution, vol. 34, no. 3, pp. 611–612, 1980.
[5]
P. R. Ehrlich and P. H. Raven, “Butterflies and plants: a study in coevolution,” Evolution, vol. 18, no. 4, pp. 586–608, 1964.
[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.
[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.
[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.
[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.
[10]
K. Groppe, T. Steinger, B. Schmid, B. Baur, and T. Boller, “Effects of habitat fragmentation on choke disease (Epichlo？ bromicola) in the grass Bromus erectus,” Journal of Ecology, vol. 89, no. 2, pp. 247–255, 2001.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[18]
L. Fahrig, “Effects of habitat fragmentation on biodiversity,” Annual Review of Ecology, Evolution, and Systematics, vol. 34, pp. 487–515, 2003.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[27]
M. Galetti, R. Guevara, M. C. C？rtes et al., “Functional extinction of birds drives rapid evolutionary changes in seed size,” Science, vol. 340, no. 6136, pp. 1086–1090, 2013.
[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.
[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.
[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.
[31]
J. N. Thompson, “Specific hypotheses on the geographic mosaic of coevolution,” American Naturalist, vol. 153, no. S5, pp. S1–S14, 1999.
[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.
[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.
[34]
T. Tscharntke and R. Brandl, “Plant-insect interactions in fragmented landscapes,” Annual Review of Entomology, vol. 49, no. 1, pp. 405–430, 2004.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[55]
A. Kruess and T. Tscharntke, “Habitat fragmentation, species loss, and biological control,” Science, vol. 264, no. 5165, pp. 1581–1584, 1994.
[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.
[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.
[58]
K. R. Crooks, “Relative sensitivities of mammalian carnivores to habitat fragmentation,” Conservation Biology, vol. 16, no. 2, pp. 488–502, 2002.
[59]
T. J. Kawecki and D. Ebert, “Conceptual issues in local adaptation,” Ecology Letters, vol. 7, no. 12, pp. 1225–1241, 2004.
[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.
[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.
[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.
[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.
[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.
[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.
[66]
S. Y. Strauss, “Floral characters link herbivores, pollinators, and plant fitness,” Ecology, vol. 78, no. 6, pp. 1640–1645, 1997.
[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.
[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.
[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.
[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.
[71]
K. Lehtil？ 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[82]
D. Fox, “Back to the no-analog future?” Science, vol. 316, no. 5826, pp. 823–825, 2007.
