Biodiversity and Conservation

, Volume 19, Issue 1, pp 257–274 | Cite as

Effects of anthropogenic habitat disturbance on local pollinator diversity and species turnover across a precipitation gradient

  • Carolina Quintero
  • Carolina Laura Morales
  • Marcelo Adrián Aizen
Original Paper
First Online:
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Accepted:

Abstract

Anthropogenic habitat disturbance can have profound effects on multiple components of forest biotas including pollinator assemblages. We assessed the effect of small-scale disturbance on local richness, abundance, diversity and evenness of insect pollinator fauna; and how habitat disturbance affected species turnover across the landscape and overall diversity along a precipitation gradient in NW Patagonia (Argentina). We evaluated the effect of disturbance on overall pollinator fauna and then separately for bees (i.e. Apoidea) and non-bee pollinators. Locally, disturbed habitats had significantly higher pollinator species richness and abundances than undisturbed habitats for the whole pollinator assemblage, but not for bees or non-bees separately. However, significant differences in species richness between habitats vanished after accounting for differences in abundance between habitat types. At a local scale Shannon–Weaver diversity and evenness did not vary with disturbance. A β diversity index indicated that, across forest types, species turnover was lower between disturbed habitats than between undisturbed habitats. In addition, rarefaction curves showed that disturbed habitats as a whole accumulated fewer species than undisturbed habitats at equivalent sample sizes. We concluded that small patches of disturbed habitat have a negligible effect on local pollinator diversity; however, habitat disturbance reduced β diversity through a homogenization of the pollinator fauna (in particular of bees) across the landscape.

Keywords

α Diversity Bees β Diversity Habitat alteration Homogenization Landscape Pollinators Rarefaction 
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Notes

Acknowledgments

We are indebted to A. Roig and G. Clapps for help on bee identification and for valuable bibliography on Diptera identification. We thank C. Nufio, Y. Linhart, M. D. Bowers, and two anonymous reviewers for their useful comments on an earlier version of this paper, and J. Paritsis for designing the map used in Fig. 1. We also thank the National Park Administration for authorizing field work in the Nahuel Huapi NP. Funding was provided by The Canon National Park Science Scholars Program for the Americas. CLM and MAA are members of Research Career of the National Research Council of Argentina (CONICET).

Supplementary material

10531_2009_9720_MOESM1_ESM.doc (64 kb)
Supplementary material 1 (DOC 64 kb)

References

  1. Aguilar R, Ashworth L, Galetto L et al (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980CrossRefPubMedGoogle Scholar
  2. Aizen MA (2007) Enfoques en el estudio de la reproducción sexual de las plantas en ambientes alterados: limitaciones y perspectivas. Aust Ecol 17:7–19Google Scholar
  3. Aizen MA, Ezcurra C (1998) High incidence of plant-animal mutualisms in the woody flora of the temperate forest of South America: biogeographical origin and present ecological significance. Aust Ecol 8:217–236Google Scholar
  4. Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine “Chaco Serrano”. Ecol Appl 4:378–392CrossRefGoogle Scholar
  5. Aizen MA, Feinsinger P (2003) Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. In: Bradshaw G, Marquet P, Mooney HA (eds) How landscapes change: human disturbance and ecosystem disruption in the Americas. Springer-Verlag, New York, pp 111–129Google Scholar
  6. Aizen MA, Vázquez DP (2006) Flower performance in human-altered habitats. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 159–179Google Scholar
  7. Aizen MA, Vázquez DP, Smith-Ramirez C (2002) Natural history and conservation of plant-animal mutualisms in the temperate forest of southern South America. Rev Chil Hist Nat 75:79–97CrossRefGoogle Scholar
  8. Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2):e31. doi: 10.1371/journal.pbio.0060031 CrossRefPubMedGoogle Scholar
  9. Amico G, Aizen MA (2000) Ecology- mistletoe seed dispersal by a marsupial. Nature 408:929–930PubMedGoogle Scholar
  10. Armesto JJ, Rozzi R, Smith-Ramirez C et al (1996) Conservation targets in South American temperate forests. Science 282:1271–1272CrossRefGoogle Scholar
  11. Beck J, Schulze CH, Linsenmair KE et al (2002) From forest to farmland: diversity of geometrid moths along two habitat gradients on Borneo. J Trop Ecol 18:33–51Google Scholar
  12. Bronstein JJ (1995) The plant-pollinator landscape. In: Hansson L, Fahrig L, Merriam G (eds) Mosaic landscapes and ecological processes. Chapman and Hall, London, pp 256–288Google Scholar
  13. Brosi BJ, Daily GC, Ehrlich PR (2007) Bee community shifts with landscape context in a tropical countryside. Ecol Appl 17:418–430CrossRefPubMedGoogle Scholar
  14. Cane J (2001) Habitat fragmentation and native bees: a premature verdict? Conserv Ecol 5: 3 [online] URL: http://www.consecol.org/vol5/iss1/art3
  15. Cane JH, Tepedino VJ (2001) Causes and extent of declines among native North American invertebrate pollinators: detection, evidence, and consequences. Conserv Ecol 5:1Google Scholar
  16. Cane JH, Minckley RL, Kervin LJ (2000) Sampling bees (Hymenoptera: Apiformes) for pollinator community studies: Pitfalls of pan-trapping. J Kans Entomol Soc 73:225–231Google Scholar
  17. Chacoff N, Aizen MA (2006) Edge effects on flower-visiting insects in grapefruit plantations bordering premontane sub-tropical forest. J Appl Ecol 43:18–27CrossRefGoogle Scholar
  18. Collinge S, Prudic K, Oliver J (2003) Effects of local habitat characteristics and landscape context on grassland butterfly diversity. Conserv Biol 17:178–187CrossRefGoogle Scholar
  19. Diaz IA, Armesto JJ, Reid S et al (2005) Linking forest structure and composition: avian diversity in successional forests of Chiloe Island, Chile. Biol Conserv 123:91–101CrossRefGoogle Scholar
  20. Dimitri MJ (1962) La flora andino-patagonica. Anales de Parques Nacionales (Buenos Aires) 9:1–115Google Scholar
  21. Dumbrell AJ, Clark EJ, Frost GA et al (2008) Changes in species diversity following habitat disturbance are dependent on spatial scale: theoretical and empirical evidence. J Appl Ecol 45:1531–1539CrossRefGoogle Scholar
  22. Echeverria C, Newton AC, Lara A et al (2007) Impacts of forest fragmentation on species composition and forest structure in the temperate landscape of southern Chile. Global Ecol Biogeogr 16:426–439CrossRefGoogle Scholar
  23. Feinsinger P, Beach JH, Linhart YB et al (1987) Disturbance, pollinator predictability, and pollination success among Costa Rica cloud forest plants. Ecology 68:1294–1305CrossRefGoogle Scholar
  24. Feinsinger P, Busby WH, Murray KG et al (1988) Mixed support for spatial heterogeneity in species interactions: hummingbirds in a tropical disturbance mosaic. Am Nat 131:33–57CrossRefGoogle Scholar
  25. Fleishman E, Betrus CJ, Blair RB (2003) Effects of spatial scale and taxonomic group on partitioning of butterfly and bird diversity in the Great Basin, USA. Landsc Ecol 18:675–685CrossRefGoogle Scholar
  26. Ghazoul J (2002) Impact of logging on the richness and diversity of forest butterflies in a tropical dry forest in Thailand. Biodivers Conserv 11:521–541CrossRefGoogle Scholar
  27. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  28. Gotelli NJ, Entsminger GL (2001) Ecosim: Null Models Software for Ecology, Version 6.0. Acquired Intelligence Inc. and Kesey-Bear. http://homepages.together.net/gentsmin/ecosim.htm
  29. Gotelli NJ, Graves RG (1996) Null models in ecology. Smithsonian Institution, Washington, DCGoogle Scholar
  30. Goulson D (2003) Bumblebees, behaviour and ecology. Oxoford University Press, NYGoogle Scholar
  31. Graham C, Blake L (2001) Influence of patch- and landscape-level factors on bird assemblages in a fragmented tropical landscape. Ecol Appl 11:1709–1721CrossRefGoogle Scholar
  32. Gray MA, Baldauf SL, Mayhew PJ et al (2007) The response of avian feeding guilds to tropical forest disturbance. Conserv Biol 21:133–141CrossRefPubMedGoogle Scholar
  33. Hamer KC, Hill JK (2000) Scale-dependent effects of habitat disturbance on species richness in tropical forests. Conserv Biol 14:1435–1440CrossRefGoogle Scholar
  34. Hatfield RG, LeBuhn G (2007) Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane meadows. Biol Conserv 139:150–158CrossRefGoogle Scholar
  35. Hegland SJ, Boeke L (2006) Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol 31:532–538CrossRefGoogle Scholar
  36. Herrera CM (1995) Microclimate and individual variation in pollinators: flowering plants are more than their flowers. Ecology 76:1516–1524CrossRefGoogle Scholar
  37. Heywood VH (1995) Global diversity assessment. Cambridge University Press, CambridgeGoogle Scholar
  38. Hill JK, Hamer KC (2004) Determining impacts of habitat modification on diversity of tropical forest fauna: the importance of spatial scale. J Appl Ecol 41:744–754CrossRefGoogle Scholar
  39. Holway DA, Lach L, Suarez AV et al (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  40. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University of Colorado Press, ColoradoGoogle Scholar
  41. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112CrossRefGoogle Scholar
  42. Koleff P, Lennon JJ, Gaston KJ (2003) Are there latitudinal gradients in species turnover? Global Ecol Biogeogr 12:483–498CrossRefGoogle Scholar
  43. Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816CrossRefPubMedGoogle Scholar
  44. Kremen C, Williams NM, Aizen MA et al (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314CrossRefPubMedGoogle Scholar
  45. Kremer C, Williams NM, Bugg RL et al (2004) The area required of an ecosystem service: crop pollination by native bee communities in California. Ecol Lett 7:1109–1119CrossRefGoogle Scholar
  46. Lande R (1996) Statistics and partitioning of species diversity and similarity among multiple communities. Oikos 76:5–13CrossRefGoogle Scholar
  47. Lennon JJ, Koleff P, Greenwood JJD et al (2001) The geographical structure of British bird distributions: diversity, spatial turnover and scale. J Anim Ecol 70:966–979CrossRefGoogle Scholar
  48. Lewis OT (2001) Effect of experimental selective logging on tropical butterflies. Conserv Biol 15:389–400CrossRefGoogle Scholar
  49. Manly BFJ (1991) Randomization, Bootstrap and Monte Carlo methods in biology. Chapman & Hall/CRC, LondonGoogle Scholar
  50. McKinney ML, Lokwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453CrossRefPubMedGoogle Scholar
  51. Memmott J, Godfray HCJ (1993) Parasitoid webs. In: Lasalle J, Gould ID (eds) Hymenoptera and biodiversity. C.A.B. International, Wallingford, pp 217–234Google Scholar
  52. Michener CD (1979) Biogeography of the bees. Annals of the Missouri Botanical Garden 66:277–347CrossRefGoogle Scholar
  53. Morales CL (2006) Alteración del hábitat e interacciones entre especies nativas y exóticas a través de la polinización en Bosques Templados de Sudamérica Austral. Tesis Doctoral. Universidad Nacional del Comahue, Bariloche, ArgentinaGoogle Scholar
  54. Morales CL, Aizen MA (2002) Does the invasion of alien plants promote invasion of alien flower visitors? A case study from the temperate forests of southern Andes. Biol Invasions 4:87–100CrossRefGoogle Scholar
  55. Morales CL, Aizen MA (2006) Invasive mutualisms and the structure of plant–pollinator interactions in the temperate forests of north-west Patagonia, Argentina. J Ecol 94:171–180CrossRefGoogle Scholar
  56. Moretti M, Duelli P, Obrist MK (2006) Biodiversity and resilience of arthropod communities after fire disturbance in temperate forests. Oecologia 149:312–327CrossRefPubMedGoogle Scholar
  57. Murcia C (1996) Forest fragmentation and the pollination of neotropical plants. In: Schelhas J, Greenberg R (eds) Forest patches in tropical landscapes. Island Press, Washington, DC, pp 19–36Google Scholar
  58. Noske NM, Hilt N, Werner FA et al (2008) Disturbance effects on diversity of epiphytes and moths in a montane forest in Ecuador. Basic Appl Ecol 9:4–12CrossRefGoogle Scholar
  59. Paritsis J, Aizen MA (2008) Effects of exotic conifer plantations on the biodiversity of understory plants, epigeal beetles and birds in Nothofagus dombeyi forests. For Ecol Manage 255:1575–1583CrossRefGoogle Scholar
  60. Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144CrossRefGoogle Scholar
  61. Pimentel D, Wilson C (1997) Economic and environmental benefits of biodiversity. Bioscience 47:112–117Google Scholar
  62. Potts SG, Vulliamy B, Dafni A et al (2003) Response of plant-pollinator communities to fire: changes in diversity, abundance and floral reward structure. Oikos 101:103–112CrossRefGoogle Scholar
  63. Rahbeck C (2005) The role of spatial scale and the perception of large-scale species-richness patterns. Ecol Lett 8:224–239Google Scholar
  64. Romey WL, Ascher JS, Powell DA et al (2007) Impacts of logging on midsummer diversity of native bees (Apoidea) in a northern hardwood forest. J Kans Entomol Soc 80:327–338CrossRefGoogle Scholar
  65. Roulston TH, Smith SA, Brewster (2007) A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. J Kans Entomol Soc 80:179–181CrossRefGoogle Scholar
  66. Sao Paulo Declaration on Pollinators (1999) Report on the recommendations of the workshop on the conservation and sustainable use of pollinators in agriculture with emphasis on bees. Brazilian Ministry of the Environment, BraziliaGoogle Scholar
  67. Simon JL (1992) Resampling stats. IBM Version 3:13Google Scholar
  68. Spagarino C, Martinez Pastur G, Peri PL (2001) Changes in Nothofagus pumilio forest biodiversity during the forest managment cycle. 1. Insects. Biodivers Conserv 10:2077–2092CrossRefGoogle Scholar
  69. Steffan-Dewenter I, Munzenberg U, Burger C et al (2002) Scale dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432CrossRefGoogle Scholar
  70. Sutherland WJ (1998) Conservation science and action. Blackwell Science Ltd., London, UKCrossRefGoogle Scholar
  71. Thompson JD (2000) How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia 126:386–394CrossRefGoogle Scholar
  72. Tscharntke T, Klein AM, Kruess A et al (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874CrossRefGoogle Scholar
  73. Tylianakis JM, Klein AM, Tscharntke T (2005) Spatiotemporal variation in the diversity of Hymenoptera across a tropical habitat gradient. Ecology 86:3296–3302CrossRefGoogle Scholar
  74. Tylianakis JM, Klein AM, Lozada T et al (2006) Spatial scale of observation affects α, β and γ diversity of cavity-nesting bees and wasps across a tropical land-use gradient. J Biogeogr 33:1295–1304CrossRefGoogle Scholar
  75. Vázquez DP, Simberloff D (2002) Ecological specialization and susceptibility to disturbance: conjectures and refutations. Am Nat 159:606–623CrossRefPubMedGoogle Scholar
  76. Vázquez DP, Simberloff D (2004) Indirect effects of an introduced ungulate on pollination and plant reproduction. Ecol Monogr 74:281–308CrossRefGoogle Scholar
  77. Veech JA, Summerville KS, Crist TO et al (2002) The additive partitioning of diversity: recent revival of an old idea. Oikos 99:3–9CrossRefGoogle Scholar
  78. Weaver W, Shannon CE (1949) The mathematical theory of communication. University of Illinois, Urbana, IllinoisGoogle Scholar
  79. Winfree R, Griswold T, Kremen C (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21:213–222CrossRefPubMedGoogle Scholar
  80. Winfree R, Aguilar R, Vázquez DP et al (2009) How do bees respond to anthropogenic disturbance? A synthesis and meta-analysis. Ecology 90:2068–2076CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Carolina Quintero
    • 1
    • 2
  • Carolina Laura Morales
    • 1
  • Marcelo Adrián Aizen
    • 1
  1. 1.Laboratorio Ecotono, Instituto de Investigaciones en Biodiversidad y Medio AmbienteUniversidad Nacional del Comahue - CONICETBariloche, Río NegroArgentina
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

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