Differential effects of anthropogenic edges and gaps on the reproduction of a forest-dwelling plant: The role of plant reproductive effort and nectar robbing by bumblebees

Austral Ecology

Volumn 37, Issue 5, 2012, Pages 600-609

  Magrach, Ainhoa ^a   Santamaría, Luis ^a   Larrinaga, Asier R ^a  

^a INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

Author keywords

Anthropogenic gap; Forest edge; Forest fragmentation; Nectar robber; Pollination

Indexed keywords

ANTAGONISM; ANTHROPOGENIC EFFECT; BEE; CLIMBING PLANT; EDGE EFFECT; ENVIRONMENTAL CHANGE; EPIPHYTE; FRUIT SET; GAP DYNAMICS; HABITAT FRAGMENTATION; NECTAR; ORNITHOPHILY; PATCH SIZE; POLLINATION; POLLINATOR; REPRODUCTIVE EFFORT; REPRODUCTIVE SUCCESS; ROBBING; SELECTIVE LOGGING; STAND STRUCTURE;

BOMBUS DAHLBOMII; MITRARIA COCCINEA; TROCHILIDAE;

EID: 84864130285     PISSN: 14429985     EISSN: 14429993     Source Type: Journal    
DOI: 10.1111/j.1442-9993.2011.02320.x     Document Type: Article

References (61)

1. Abd Latif Z. & Blackburn G. A. (2010) The effects of gap size on some microclimate variables during late summer and autumn in a temperate broadleaved deciduous forest. Int. J. Biometeorol. 54, 119-29.
2. Amico G. C. & Aizen M. A. (2005) Dispersión de semillas por aves en un bosque templado de Sudamérica austral: ¿quién dispersa a quién? Ecol. Austral 15, 89-100.
3. Aoyagi Y. & Akimoto M. (2009) Reactive shifts in the pattern of resource allocation in three Lolium species with different levels of persistency under clipping disturbance. Grassl. Sci. 55, 181-6.
4. Armesto J. J. & Figueroa J. (1987) Stand structure and dynamics in the temperate rain forests of Chiloé Archipelago, Chile. J. Biogeogr. 14, 367-76.
5. Bierregaard R. O., Lovejoy T. E. Jr, Kapos V., Santos A. A. & Hutchings R. W. (1992) The biological dynamics of tropical rainforest fragments. Bioscience 42, 859-66.
6. Buckland S. T. (2006) Point transect surveys for songbirds: robust methodologies. Auk 123, 345-57.
7. Buckland S. T., Anderson D. R., Burnham K. P., Laake J. L., Borchers D. L. & Thomas L. (2004) Advanced Distance Sampling. Estimating Abundance of Biological Populations. Oxford University Press, New York.
8. Burgess V., Kelly D., Robertson A. W. & Ladley J. J. (2006) Positive effects of forest edges on plant reproduction: literature review and a case study of bee visitation to flowers of Peraxilla tetrapetala (Loranthaceae). N.Z. J. Ecol. 30, 179-90.
9. Burnham K. M. & Lee T. D. (2010) Canopy gaps facilitate establishment, growth and reproduction of invasive Frangula alnus in a Tsuga canadensis dominated forest. Biol. Invasions 12, 1509-20.
10. Christianini A. V. & Galetti M. (2007) Spatial variation in post-dispersal seed removal in an Atlantic forest: effects of habitat, location and guilds of seed predators. Acta Oecol. 32, 328-36.
11. Cordeiro N. J. & Howe H. F. (2001) Low recruitment of trees dispersed by animals in African forest fragments. Conserv. Biol. 15, 1733-41.
12. Díaz I. A., Armesto J. J., Reid S., Sieving K. E. & Willson M. F. (2005) Linking forest structure and composition: avian diversity in successional forests of Chiloé Island, Chile. Biol. Conserv. 123, 91-101.
13. Donoso D., Grez A. A. & Simonetti J. A. (2003) Effects of forest fragmentation on the granivory of differently sized seeds. Biol. Conserv. 115, 63-70.
14. Echeverría C., Coomes D. A., Hall M. & Newton A. C. (2008) Spatially explicit models to analyze forest loss and fragmentation between 1976 and 2020 in southern Chile. Ecol. Modell. 212, 439-49.
15. Fahrig L. (2003) Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487-515.
16. Feinsinger P., Busby W. H., Murray K. G., Beach J. H., Pounds W. Z. & Linhart Y. B. (1988) Mixed support for spatial heterogeneity in species interactions: hummingbirds in a tropical disturbance mosaic. Am. Nat. 131, 33-57.
17. Fischer J. & Lindenmayer D. B. (2007) Landscape modification and habitat fragmentation: a synthesis. Glob. Ecol. Biogeogr. 16, 265-80.
18. Foley J. A., DeFries R., Asner G. P. etal. (2005) Global consequences of land use. Science 309, 570-4.
19. García D. & Chacoff N. P. (2007) Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory, and seed predation. Conserv. Biol. 21, 400-11.
20. Harper K. A., Macdonald S. E., Burton P. J. etal. (2005) Edge influence on forest structure and composition in fragmented landscapes. Conserv. Biol. 19, 768-82.
21. Herrera C. M., Medrano M., Rey P. J. etal. (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc. Natl. Acad. Sci. U.S.A. 99, 16823-8.
22. Irwin R. E. & Brody A. K. (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116, 519-27.
23. Irwin R. E., Brody A. K. & Waser N. M. (2001) The impact of floral larceny on individuals, populations and communities. Oecologia 129, 161-8.
24. Jules E. S. & Rathcke B. J. (1999) Mechanisms of reduced Trillium recruitment along edges of old-growth forest fragments. Conserv. Biol. 13, 784-93.
25. Karban R. & Strauss S. Y. (1993) Effects of herbivores on growth and reproduction of their perennial host, Erigeron glaucus. Ecology 74, 39-46.
26. Kelly D., Ladley J. J. & Robertson A. W. (2008) Flower predation by Zelleria maculata (Lepidoptera) on Peraxilla mistletoes: effects of latitude and fragmentation, and impact on fruit set. N.Z. J. Ecol. 32, 186-96.
27. Klink C. A. & Machado R. B. (2005) Conservation of the Brazilian Cerrado. Conserv. Biol. 19, 707-13.
28. Lang S. & Tiede D. (2003) vLATE Extension für ArcGIS - vektorbasiertes Tool zur quantitativen Landschaftsstrukturanalyse. ESRI Anwenderkonferenz, Innsbruck.
29. Lara A., Echeverría C. & Reyes R. (2002) Bosques. In: Informe Pais: Estado del Medio Ambiente en Chile-2002 (ed. Centro de Analisis de Politicas Publicas) pp. 131-60. Universidad de Chile, Santiago.
30. McGarigal K., Cushman S. A., Neel M. C. & Ene E. (2002) FRAGSTATS: Spatial Pattern Analysis Program for Categorical Maps (computer software program). Available at: (accessed 21 December 2008).
31. Magrach A., Larrinaga A. R. & Santamaría L. (2011) Changes in patch features may exacerbate or compensate for the effect of habitat loss on forest bird populations. PLoS ONE 6, e21596.
32. Maloof J. E. (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am. J. Bot. 88, 1960-5.
33. Maloof J. E. & Inouye D. W. (2000) Are nectar robbers cheaters or mutualists? Ecology 81, 2651-61.
34. Mitchell B. (2007) FragStatsBatch for ArcGIS 9 (software). Available at: (accessed 10 January 2009).
35. Morris W. F. (1996) Mutualism denied? Nectar-robbing bumble bees do not reduce female or male success of bluebells. Ecology 77, 1451-62.
36. Mothershead K. & Marquis R. J. (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81, 30-40.
37. Murcia C. (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol. Evol. 10, 58-62.
38. Murcia C. (1996) Forest fragmentation and the pollination of neotropical plants. In: Forest Patches in Tropical Landscapes (eds J. Schelhas & R. Greenberg ) pp. 19-36. Island Press, Washington.
39. Nunes Ramos F. & Maës Santos F. A. (2006) Floral visitors and pollination of Psychotria tenuinervis (Rubiaceae): distance from the anthropogenic and natural edges of an Atlantic forest fragment. Biotropica 38, 383-9.
40. Nunes Ramos F., Feliciano de Lima P., Zucchi M. I., Colombo C. A. & Solferini V. N. (2010) Genetic structure of tree and shrubby species among anthropogenic edges, natural edges and interior of an Atlantic forest fragment. Biochem. Genet. 48, 215-28.
41. Olson D. M. & Dinerstein E. (1998) The Global 200: a representation approach to conserving the Earth's most biologically valuable ecoregions. Conserv. Biol. 12, 502-15.
42. Osborne J. L., Martin A. P., Shorthall C. R. etal. (2007) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J. Appl. Ecol. 45, 784-92.
43. Rangel T. F. L. V. B., Diniz-Filho J. A. F. & Bini L. M. (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Glob. Ecol. Biogeogr. 15, 321-7.
44. Rebolledo R. R., Martinez H. P., Palma M. R., Aguilera A. P. & Klein C. K. (2004) Actividad de visita de Bombus dahlbomii (Guérin) y Bombus ruderatus (F.) (Himenoptera: Apidae) sobre trébol rosado (Trifolium pratense L.). Agric. Tecn. (Chile) 64, 245-50.
45. Restrepo C. & Vargas A. (1999) Seeds and seedlings of two neotropical montane understory shrubs respond differently to anthropogenic edges and treefall gaps. Oecologia 119, 419-26.
46. Rozzi R., Martinez D., Willson M. F. & Sabag C. (1996) La avifauna de los bosques templados de Sudamerica. In: Ecologia de los bosques nativos de Chile (eds J. J. Armesto, C. Villagran & M. T. K. Arroyo ) pp. 135-52. Editorial Universitaria, Santiago.
47. Salinas M. F. (2008) Diferenciacion de nichos ecologicos de tres especies de gesneriaceas epifitas del bosque templado del sur de Chile. PhD Dissertation. Universidad de Chile.
48. Saunders D. A., Hobbs R. J. & Margules C. R. (1991) Biological consequences of ecosystem fragmentation: a review. Conserv. Biol. 5, 18-32.
49. Siepieslki A. M. & Benkman C. W. (2009) Conflicting selection from an antagonist and a mutualist enhances phenotypic variation in a plant. Evolution 64, 1120-8.
50. Smith-Ramirez C. (1993) Los picaflores y su recurso floral en el bosque templado de la isla de Chiloé, Chile. Rev. Chil. Hist. Nat. 66, 65-73.
51. Smith-Ramirez C., Martinez P., Nuñez M., Gonzalez C. & Armesto J. J. (2005) Diversity, flower visitation frequency and generalism of pollinators in temperate rain forests of Chiloé Island, Chile. Bot. J. Linn. Soc. 147, 399-416.
52. Sodhi N. S., Koh L. P., Brook B. W. & Ng P. K. L. (2004) Southeast Asian biodiversity: an impending disaster. Trends Ecol. Evol. 19, 654-60.
53. Strauss S. Y. (1997) Floral characters link herbivores, pollinators and plant fitness. Ecology 78, 1640-5.
54. Thomas L., Laake J. L., Strindberg S. etal. (2006) Distance 5.0. Release 'x'1. Research Unit for Wildlife Population Assessment, University of St. Andrews, UK. Available at: (accessed 23 March 2009).
55. Traveset A., Willson M. F. & Sabag C. (1998) Effect of nectar-robbing birds on fruit set of Fuchsia magellanica in Tierra del Fuego: a disrupted mutualism. Funct. Ecol. 12, 459-64.
56. Urcelay C., Morales C. L. & Chalcoff V. R. (2006) Relationship between corolla length and floral larceny in the South American hummingbird-pollinated Campsidium valdivianum (Bignoniaceae). Ann. Bot. Fenn. 43, 205-11.
57. Van Zandt P. A., Tobler M. A., Mouton E., Hasenstein K. H. & Mopper S. (2003) Positive and negative consequences of salinity stress for the growth and reproduction of the clonal plant Iris hexagona. J. Ecol. 91, 837-46.
58. Willson M. F., Irvine A. K. & Walsh N. G. (1989) Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21, 133-47.
59. Willson M. F., De Santo T. L., Sabag C. & Armesto J. J. (1994) Avian communities of fragmented south-temperate rainforests in Chile. Conserv. Biol. 8, 508-20.
60. Winfree R., Griswold T. & Kremen C. (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv. Biol. 21, 213-23.
61. Winfree R., Aguilar R., Vázquez D. P., Lebuhn G. & Aizen M. A. (2009) A meta-analysis of bees' responses to anthropogenic disturbance. Ecology 90, 2068-76.