Oecologia

, Volume 176, Issue 2, pp 465–476 | Cite as

Floral neighborhood influences pollinator assemblages and effective pollination in a native plant

Plant-microbe-animal interactions - Original research

Abstract

Pollinators represent an important intermediary by which different plant species can influence each other’s reproductive fitness. Floral neighbors can modify the quantity of pollinator visits to a focal species but may also influence the composition of visitor assemblages that plants receive leading to potential changes in the average effectiveness of floral visits. We explored how the heterospecific floral neighborhood (abundance of native and non-native heterospecific plants within 2 m × 2 m) affects pollinator visitation and composition of pollinator assemblages for a native plant, Phacelia parryi. The relative effectiveness of different insect visitors was also assessed to interpret the potential effects on plant fitness of shifts in pollinator assemblage composition. Although the common non-native Brassica nigra did not have a significant effect on overall pollinator visitation rate to P. parryi, the proportion of flower visits that were made by native pollinators increased with increasing abundance of heterospecific plant species in the floral neighborhood other than B. nigra. Furthermore, native pollinators deposited twice as many P. parryi pollen grains per visit as did the nonnative Apis mellifera, and visits by native bees also resulted in more seeds than visits by A. mellifera. These results indicate that the floral neighborhood can influence the composition of pollinator assemblages that visit a native plant and that changes in local flower communities have the potential to affect plant reproductive success through shifts in these assemblages towards less effective pollinators.

Keywords

Pollinator visitation Honeybees Invasive species Native bees Pollinator effectiveness 

References

  1. Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honeybees in Argentine Chaco Serrano. Ecol Appl 4:378–392. doi:10.2307/1941941 CrossRefGoogle Scholar
  2. Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:396–403. doi:10.2307/1941941 CrossRefGoogle Scholar
  3. Ashman TL, Arceo-Gómez G (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am J Bot 100:1061–1070. doi:10.3732/ajb.1200496 PubMedCrossRefGoogle Scholar
  4. Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387. doi:10.1073/pnas.1633576100 PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bell DT, Muller CH (1973) Dominance of California annual grasslands by Brassica nigra. Am Midl Nat 90:277–299. doi:10.2307/2424453 CrossRefGoogle Scholar
  6. Bell JM, Karron JD, Mitchell RJ (2005) Interspecific competition for pollination lowers seed production and outcrossing in Mimulus ringens. Ecology 86:762–771. doi:10.2307/3450670 CrossRefGoogle Scholar
  7. Benedek P, Nyeki J (1996) Pollinating efficiency of honeybees on apple cultivars as affected by their flower characteristics. Hortic Sci 28:40–47Google Scholar
  8. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemueller R, Edwards M, Peeters T, Kunin WE, et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354. doi:10.1126/science.1127863 PubMedCrossRefGoogle Scholar
  9. Bjerknes AL, Totland O, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12. doi:10.1016/j.biocon.2007.04.015 CrossRefGoogle Scholar
  10. Bond WJ (1994) Do mutualisms matter—assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc B Biol Sci 344:83–90. doi:10.1098/rstb.1994.0055 CrossRefGoogle Scholar
  11. Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336. doi:10.2307/3072063 CrossRefGoogle Scholar
  12. Campbell DR, Motten AF (1985) The mechanism of competition for pollination between two forest herbs. Ecology 66:554–563. doi:10.2307/3072063 CrossRefGoogle Scholar
  13. Canto-Aguilar MA, Parra-Tabla V (2000) Importance of conserving alternative pollinators: assessing the pollination efficiency of the squash bee, Peponapis limitaris in Cucurbita moschata (Cucurbitaceae). J Insect Conserv 4:203–210CrossRefGoogle Scholar
  14. Chittka L, Schurkens S (2001) Successful invasion of a floral market. Nature 411:653. doi:10.1038/35079676 PubMedCrossRefGoogle Scholar
  15. Conner JK, Neumeier R (1995) Effects of black mustard population size on the taxonomic composition of pollinators. Oecologia 104:218–224. doi:10.1007/BF00328586 CrossRefGoogle Scholar
  16. Covich A (1974) Ecological economics of foraging among coevolving animals and plants. Ann Mo Bot Gard 61:794–805. doi:10.2307/2395030 CrossRefGoogle Scholar
  17. Eickwort GC, Ginsberg HS (1980) Foraging and mating behavior in Apoidea. Annu Rev Entomol 25:421–446. doi:10.1146/annurev.en.25.010180.002225 CrossRefGoogle Scholar
  18. Feinsinger P, Tiebout HM (1991) Competition among plants sharing hummingbird pollinators: laboratory experiments on a mechanism. Ecology 72:1946–1952. doi:10.2307/1941549 CrossRefGoogle Scholar
  19. Feldman TS, Morris WF, Wilson WG (2004) When can two species facilitate each other’s pollination? Oikos 105:197–207CrossRefGoogle Scholar
  20. Flanagan RJ, Mitchell RJ, Karron JD (2010) Increased relative abundance of an invasive competitor for pollination, Lythrum salicaria, reduces seed number in Mimulus ringens. Oecologia 164:445–454. doi:10.1007/s00442-010-1693-2 PubMedCrossRefGoogle Scholar
  21. Freitas BM, Paxton RJ (1998) A comparison of two pollinators: the introduced honey bee Apis mellifera and an indigenous bee Centris tarsata on cashew Anacardium occidentale in its native range of NE Brazil. J Appl Ecol 35:109–121. doi:10.1046/j.1365-2664.1998.00278.x CrossRefGoogle Scholar
  22. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Klein AM, et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. doi:10.1126/science.1230200 PubMedCrossRefGoogle Scholar
  23. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764. doi:10.1046/j.1365-2656.2002.00641.x CrossRefGoogle Scholar
  24. Goulson D (2003) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34:1–26. doi:10.1146/annurev.ecolsys.34.011802.132355 CrossRefGoogle Scholar
  25. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. doi:10.1007/s00442-007 PubMedCrossRefGoogle Scholar
  26. Gross CL, Mackay D (1998) Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol Conserv 86:169–178. doi:10.1016/S0006-3207(98)00010-X CrossRefGoogle Scholar
  27. 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 31:532–538. doi:10.1111/j.1365-2311.2006.00812.x CrossRefGoogle Scholar
  28. Heinrich B (1979) Bumblebee economics. Harvard University Press, CambridgeGoogle Scholar
  29. Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597–602. doi:10.1126/science.176.4035.597 PubMedCrossRefGoogle Scholar
  30. Hill PSM, Wells PH, Wells H (1997) Spontaneous flower constancy and learning in honey bees as a function of colour. Anim Behav 54:615–627. doi:10.1006/anbe.1996.0467 PubMedCrossRefGoogle Scholar
  31. Hopwood JL (2008) The contribution of roadside grassland restorations to native bee conservation. Biol Conserv 141:2632–2640. doi:10.1016/j.biocon.2008.07.026 CrossRefGoogle Scholar
  32. Huryn VMB (1997) Ecological impacts of introduced honey bees. Q Rev Biol 72:275–297. doi:10.1086/419860 CrossRefGoogle Scholar
  33. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  34. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112. doi:10.1146/annurev.ecolsys.29.1.83 CrossRefGoogle Scholar
  35. Keys RN, Buchmann SL, Smith SE (1995) Pollination effectiveness and pollination efficiency of insects foraging Prosopis velutina in south-eastern Arizona. J Appl Ecol 32:519–527. doi:10.2307/2404649 CrossRefGoogle Scholar
  36. Kremen C, Ricketts T (2000) Global perspectives on pollination disruptions. Conserv Biol 14:1226–1228. doi:10.1046/j.1523-1739.2000.00013.x CrossRefGoogle Scholar
  37. Lankau R (2008) A chemical trait creates a genetic trade-off between intra and interspecific competitive ability. Ecology 89:1181–1187. doi:10.1890/07-1541.1 PubMedCrossRefGoogle Scholar
  38. Lankau RA, Strauss SY (2007) Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317:1561–1563. doi:10.1126/science.1147455 PubMedCrossRefGoogle Scholar
  39. Larson DL, Royer RA, Royer MR (2006) Insect visitation and pollen deposition in an invaded prairie plant community. Biol Conserv 130:148–159. doi:10.1016/j.biocon.2005.12.009 CrossRefGoogle Scholar
  40. Laverty TM (1992) Plant interactions for pollinator visits—a test of the magnet species effect. Oecologia 89:502–508Google Scholar
  41. Lázaro A, Lundgren R, Totland Ø (2009) Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos 118:691–702. doi:10.1111/j.1600-0706.2008.17168.x CrossRefGoogle Scholar
  42. McGregor SE (1976) Insect pollination of cultivated crop plants. Agricultural handbook no. 496. USDA, Agricultural Research Service, Washington, DCGoogle Scholar
  43. McGregor SE, Alcorn EB, Kuitz EB Jr, Butler GD Jr (1959) Bee visitors to saguaro flowers. J Econ Entomol 52:1002–1004Google Scholar
  44. McKinney AM, Goodell K (2010) Shading by invasive shrub reduces seed production and pollinator services in a native herb. Biol Invasions 12:2751–2763. doi:10.1007/s10530-009-9680-4 CrossRefGoogle Scholar
  45. Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proc R Soc B Biol Sci 269:2395–2399. doi:10.1098/rspb.2002.2174 CrossRefGoogle Scholar
  46. Moeller DA (2005) Pollinator community structure and sources of spatial variation in plant-pollinator interactions in Clarkia xantiana ssp. xantiana. Oecologia 142:28–37. doi:10.2307/20062133 PubMedCrossRefGoogle Scholar
  47. Molina-Montenegro MA, Badano EI, Cavieres LA (2008) Positive interactions among plant species for pollinator service: assessing the ‘magnet species’ concept with invasive species. Oikos 117:1833–1839. doi:10.1098/rspb.2002.2174 CrossRefGoogle Scholar
  48. Moragues E, Traveset A (2005) Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands. Biol Conserv 122:611–619. doi:10.1016/j.biocon.2004.09.015 CrossRefGoogle Scholar
  49. 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 94:171–180. doi:10.1111/j.1365-2745.2005.01069.x CrossRefGoogle Scholar
  50. Morales C, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. CRC Crit Rev Plant Sci 27:221–238. doi:10.1080/07352680802205631 CrossRefGoogle Scholar
  51. Muller CH (1969) Allelopathy as a factor in ecological process. Vegetation 16:348–357CrossRefGoogle Scholar
  52. Munoz AA, Cavieres LA (2008) The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities. J Ecol 96:459–467. doi:10.1111/j.1365-2745.2008.01361.x CrossRefGoogle Scholar
  53. Murcia C, Feinsinger P (1996) Interspecific pollen loss by hummingbirds visiting flower mixtures: effects of floral architecture. Ecology 77:550–560. doi:10.2307/2265629 CrossRefGoogle Scholar
  54. Natural Research Council (2006) Status of pollinators in North America. National Academic Press, Washington, DCGoogle Scholar
  55. Ne’eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev Camb Philos Soc 85:435–451. doi:10.1111/j.1469-185X.2009.00108.x PubMedGoogle Scholar
  56. Oduor AMO, Lankau RA, Strauss SY, Gomez JM (2011) Introduced Brassica nigra populations exhibit greater growth and herbivore resistance but less tolerance than native populations in the native range. New Phytol 191:536–544. doi:10.1111/j.1469-8137.2011.03685.x PubMedCrossRefGoogle Scholar
  57. Paton DC (1993) Honeybees in the Australian environment: does Apis mellifera disrupt or benefit the native biota? Bioscience 43:95–103CrossRefGoogle Scholar
  58. Potts SG, Vulliamy B, Dafni A, Ne’eman G, Willmer P (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84:2628–2642. doi:10.1890/02-0136 CrossRefGoogle Scholar
  59. Primack RB, Silander JA (1975) Measuring the relative importance of different pollinators to plants. Nature 255:143–144. doi:10.1111/j.1362311.1994.tb00419.x CrossRefGoogle Scholar
  60. Rejmanek M, Richardson DM, Pysek P (2005) Plant invasions and invasibility of plant communities. In: van der Maarel E (ed) Veg ecol. Blackwell, Oxford, pp 332–355Google Scholar
  61. Richards KW (1996) Comparative efficacy of bee species for pollination of legume seed crops. In: Matheson A, O’Toole C, Williams I, Buchmann SL, Westrich P (eds) The conservation of bees (Linnean Society Symposium Series). Academic Press, London, pp 81–104Google Scholar
  62. Roberts RH (1945) Blossom structure and setting of delicious and other apple varieties. Proc Am Soc For Hortic Sci 46:87–90Google Scholar
  63. Roubik DW (1996) African honey bees as exotic pollinators in French Guiana. In: Matheson A, et al. (eds) The conservation of bees. Academic Press, London, pp 173–182Google Scholar
  64. Rymer PD, Whelan RJ, Ayre DJ, Weston PH, Russell KG (2005) Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae). Biol Conserv 123:521–532. doi:10.1016/j.biocon.2005.01.002 CrossRefGoogle Scholar
  65. Schoenherr AA (1992) A natural history of California. University of California Press, BerkeleyGoogle Scholar
  66. Steffan-Dewenter I, Schiele S (2008) Do resources or natural enemies drive bee population dynamics in fragmented habitats? Ecology 89:1375–1387. doi:10.2307/3071954 PubMedCrossRefGoogle Scholar
  67. Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst 35:435–466. doi:10.1146/annurev.ecolsys.35.112202.130215 CrossRefGoogle Scholar
  68. Suzuki K, Dohzono I, Hiei K, Fukuda Y (2002) Pollination effectiveness of the three bumblebee species on flowers of Hosta sieboldiana (Liliaceae) and its relation to floral structure and pollinator size. Plant Species Biol 17:139–146CrossRefGoogle Scholar
  69. Thomson JD, Goodell K (2001) Pollen removal and deposition by honeybee and visitors to apple and almond flowers. J Appl Ecol 38:1032–1044. doi:10.1046/j.1365-2664.2001.00657.x CrossRefGoogle Scholar
  70. vanEngelsdorp D, Hayes Jr J, Underwood RM, Pettis J (2008) A survey of honey bee colony losses in the US, fall 2007 to spring 2008. PLoS One 3(12). doi: 10.1371/journal.pone.0004071
  71. Waddington KD (1976) Foraging patterns of halictid bees at flowers of Convolvulus arvensis. Psyche 83:12–19CrossRefGoogle Scholar
  72. Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two colorado wildflowers. Ecology 59:934–944. doi:10.2307/1938545 CrossRefGoogle Scholar
  73. Waser NM (1986) Flower constancy—definition, cause, and measurement. Am Nat 127:593–603. doi:10.1086/284507 CrossRefGoogle Scholar
  74. Waser NM, Price MV (1990) Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting Delphinium nelsonii. Collect Bot 19:9–20CrossRefGoogle Scholar
  75. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. doi:10.2307/2265575 CrossRefGoogle Scholar
  76. Watts S, Huaman Ovalle D, Moreno Herrera M, Ollerton J (2012) Pollinator effectiveness of native and non-native flower visitors to an apparently generalist Andean shrub, Duranta mandonii (Verbenaceae). Plant Species Biol 27:147–158. doi:10.1111/j.1442-1984.2011.00337.x CrossRefGoogle Scholar
  77. Wells H, Wells PH (1983) Honey bee foraging ecology—optimal diet, minimal uncertainty or individual constancy. J Anim Ecol 52:829–836. doi:10.2307/4457 CrossRefGoogle Scholar
  78. Westerkamp C (1991) Honeybees are poor pollinators—why? Plant Syst Evol 177:71–75. doi:10.1007/BF00937827 CrossRefGoogle Scholar
  79. Westerling AL, Bryant BP, Preisler HK, Holmes TP, Hidalgo HG, Das T, Shrestha SR (2011) Climate change and growth scenarios for California wildfire. Clim Change 109:445–463. doi:10.1007/s10584-011-0329-9 CrossRefGoogle Scholar
  80. Western Regional Climate Center (2013) Cooperative climatological data summaries.http://www.wrcc.dri.edu/climatedata/climsum/.cited 2013
  81. Westman AL, Kresovich S, Dickson MH (1999) Regional variation in Brassica nigra and other weedy crucifers for disease reaction to Alternaria brassicicola and Xanthomonas campestris pv. campestris. Euphytica 106:253–259. doi:10.1023/A:1003544025146 CrossRefGoogle Scholar
  82. Weston LA (1996) Utilization of allelopathy for weed management in agroecosystems. Agron J 88:860–866CrossRefGoogle Scholar
  83. Willmer PG, Bataw AAM, Hughes JP (1994) The superiority of bumblebees to honeybees as pollinators: insect visits to raspberry flowers. Ecol Entomol 19:271–284. doi:10.1111/j.1365-2311.1994.tb00419.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA

Personalised recommendations