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.
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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
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:396–403. doi:10.2307/1941941
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
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
Bell DT, Muller CH (1973) Dominance of California annual grasslands by Brassica nigra. Am Midl Nat 90:277–299. doi:10.2307/2424453
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
Benedek P, Nyeki J (1996) Pollinating efficiency of honeybees on apple cultivars as affected by their flower characteristics. Hortic Sci 28:40–47
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
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
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
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
Campbell DR, Motten AF (1985) The mechanism of competition for pollination between two forest herbs. Ecology 66:554–563. doi:10.2307/3072063
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 4:203–210
Chittka L, Schurkens S (2001) Successful invasion of a floral market. Nature 411:653. doi:10.1038/35079676
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
Covich A (1974) Ecological economics of foraging among coevolving animals and plants. Ann Mo Bot Gard 61:794–805. doi:10.2307/2395030
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
Feinsinger P, Tiebout HM (1991) Competition among plants sharing hummingbird pollinators: laboratory experiments on a mechanism. Ecology 72:1946–1952. doi:10.2307/1941549
Feldman TS, Morris WF, Wilson WG (2004) When can two species facilitate each other’s pollination? Oikos 105:197–207
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
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
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
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
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
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
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
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
Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge
Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597–602. doi:10.1126/science.176.4035.597
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
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
Huryn VMB (1997) Ecological impacts of introduced honey bees. Q Rev Biol 72:275–297. doi:10.1086/419860
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot
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
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
Kremen C, Ricketts T (2000) Global perspectives on pollination disruptions. Conserv Biol 14:1226–1228. doi:10.1046/j.1523-1739.2000.00013.x
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
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
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
Laverty TM (1992) Plant interactions for pollinator visits—a test of the magnet species effect. Oecologia 89:502–508
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
McGregor SE (1976) Insect pollination of cultivated crop plants. Agricultural handbook no. 496. USDA, Agricultural Research Service, Washington, DC
McGregor SE, Alcorn EB, Kuitz EB Jr, Butler GD Jr (1959) Bee visitors to saguaro flowers. J Econ Entomol 52:1002–1004
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
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
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
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
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
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
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
Muller CH (1969) Allelopathy as a factor in ecological process. Vegetation 16:348–357
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
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
Natural Research Council (2006) Status of pollinators in North America. National Academic Press, Washington, DC
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
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
Paton DC (1993) Honeybees in the Australian environment: does Apis mellifera disrupt or benefit the native biota? Bioscience 43:95–103
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
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
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 332–355
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 81–104
Roberts RH (1945) Blossom structure and setting of delicious and other apple varieties. Proc Am Soc For Hortic Sci 46:87–90
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 173–182
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
Schoenherr AA (1992) A natural history of California. University of California Press, Berkeley
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
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
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 17:139–146
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
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
Waddington KD (1976) Foraging patterns of halictid bees at flowers of Convolvulus arvensis. Psyche 83:12–19
Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two colorado wildflowers. Ecology 59:934–944. doi:10.2307/1938545
Waser NM (1986) Flower constancy—definition, cause, and measurement. Am Nat 127:593–603. doi:10.1086/284507
Waser NM, Price MV (1990) Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting Delphinium nelsonii. Collect Bot 19:9–20
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
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
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
Westerkamp C (1991) Honeybees are poor pollinators—why? Plant Syst Evol 177:71–75. doi:10.1007/BF00937827
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
Western Regional Climate Center (2013) Cooperative climatological data summaries.http://www.wrcc.dri.edu/climatedata/climsum/.cited 2013
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
Weston LA (1996) Utilization of allelopathy for weed management in agroecosystems. Agron J 88:860–866
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
Acknowledgments
This research was funded by University of California Irvine’s Center for Environmental Biology. We thank the Irvine Ranch Conservancy and OC Parks for granting access to field sites. We are also grateful to our undergraduate assistants, Grace Yu, Rachel Finer and Kenneth Chang, and to Steve Weller, Kailen Mooney, and two anonymous reviewers for providing feedback on manuscript drafts.
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Bruckman, D., Campbell, D.R. Floral neighborhood influences pollinator assemblages and effective pollination in a native plant. Oecologia 176, 465–476 (2014). https://doi.org/10.1007/s00442-014-3023-6
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DOI: https://doi.org/10.1007/s00442-014-3023-6