Abstract
Marginal grassland fragments, such as road verges and field margins, may act as important supplemental habitats for grassland plants in the modern agricultural landscape. However, abundance of pollinators in such fragments has been found to decline with distance to larger natural and semi-natural habitats, and this could have corresponding effects on plant pollination. In this study, we performed a field experiment on road verges with three insect-pollinated grassland herbs to examine the relationship between distance to semi-natural grassland and plant reproductive success in two landscapes with contrasting farming intensities. In Lychnis viscaria and Lotus corniculatus, seed production tended to decrease with increasing distance to semi-natural grassland, but only in the landscape with high farming intensity. Seed production in Armeria maritima spp. maritima decreased with distance in both landscapes. Although many studies have investigated effects of natural habitat on crop pollination, little is known about the impact on pollination in native plants. The results from this study indicate that management of semi-natural grasslands improves not only biodiversity within the actual grassland but also pollination of native plants in the surrounding agricultural landscape.
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References
Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790
Ågren J, Ehrlén J, Solbreck C (2008) Spatio-temporal variation in fruit production and seed predation in a perennial herb influenced by habitat quality and population size. J Ecol 96:334–345
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980
Allen-Wardell G, Berhardt P, Bitner R, Burquez A et al (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Biol Conserv 12:8–17
Angeloni F, Ouborg J, Leimu R (2011) Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol Conserv 144:35–43
Ashman TL, Knight TM, Steets JA et al (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421
Auestad I, Rydgren K, Auestad I (2011) Road verges: potential refuges for declining grassland species despite remnant vegetation dynamics. Ann Bot Fenn 48:289–303
Bartomeus I, Montserrat Vilà M, Steffan-Dewenter I (2010) Combined effects of Impatiens glandulifera invasion and landscape structure on native plant pollination. J Ecol 98:440–450
Biesmeijer JC et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354
Bommarco R, Kleijn D, Potts SD (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238
Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed. Bot Rev 60:83–139
Corbet SA (1995) Insects, plants and succession: advantages of long-term set-aside. Agric Ecosyst Environ 53:201–217
Cousins SAO (2006) Plant species richness in midfield islets and road verges—the effect of landscape fragmentation. Biol Conserv 127:500–509
Cousins SAO (2009) Landscape history and soil properties affect grassland decline and plant species richness in rural landscapes. Biol Conserv 142:2752–2758
Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond B 267:1149–1152
Dauber J et al (2010) Effects of patch size and density on flower visitation and seed set of wild plants: a pan-European approach. J Ecol 98:188–196
Ekroos J, Rundlöf M, Smith HG (2013) Trait-dependent responses of flower-visiting insects to distance to semi-natural grasslands and landscape heterogeneity. Landscape Ecol. doi:10.1007/s10980-013-9864-2
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242
Eriksson O, Cousins SAO, Bruun HH (2002) Land-use history and fragmentation of traditionally managed grasslands in Scandinavia. J Veg Sci 13:743–748
Garibaldi LA et al (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072
Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. Ecology 71:757–764
Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208
Goverde M, Schweizer K, Erhardt BBA (2002) Small-scale habitat fragmentation effects on pollinator behaviour: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands. Biol Conserv 104:293–299
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596
Holzschuh A, Dudenhoffer J-H, Teja Tscharntke T (2012) Landscapes with wild bee habitats enhance pollination, fruit set and yield of sweet cherry. Biol Conserv 153:101–107
Jakobsson A, Padron B (2013) Do the invasive Lupinus polyphyllus increase pollinator visitation to a native herb through effects on pollinator population sizes? Oecologia. doi:10.1007/s00442-013-2756-y
Jantunen J, Saarinen K, Valtonen A, Saarnio S (2007) Flowering and seed production success along roads with different mowing regimes. Appl Veg Sci 10:285–292
Jauker F, Diekötter T, Schwarzbach F, Wolters V (2009) Pollinator dispersal in an agricultural matrix: opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landsc Ecol 24:547–555
Jones DA, Turkington R (1986) Biological flora of the British Isles no. 195 Lotus corniculatus L. J Ecol 74:1185–1212
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112
Kells AR, Goulson D (2003) Preferred nesting sites of bumblebee queens (Hymenoptera: Apidae) in agroecosystems in the UK. Biol Conserv 109:165–174
Kleijn D, van Langevelde F (2006) Interacting effects of landscape context and habitat quality on flower visiting insects in agricultural landscapes. Basic Appl Ecol 7:201–214
Klein A-M, Brittain C, Hendrix SD, Thorp R, Williams N, Kremen C (2012) Wild pollination services to California almond rely on semi-natural habitat. J Appl Ecol 49:723–732
Kolb A, Ehrlén J, Eriksson O (2007) Ecological and evolutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspect Plant Ecol Evol Syst 9:79–100
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816
Krewenka KM, Holzschuh A, Tscharntke T, Dormann CF (2011) Landscape elements as potential barriers and corridors for bees, wasps and parasitoids. Biol Conserv 144:1816–1825
Krishnan S, Kushalappa CG, Shaanker RU, Ghazoul J (2012) Status of pollinators and their efficiency in coffee fruit set in a fragmented landscape mosaic in South India. Basic Appl Ecol 13:277–285
Kull K, Zobel M (1991) High species richness in an Estonian wooded meadow. J Veg Sci 2:711–714
Kwak M, Jennersten O (1986) The significance of pollination time and frequency, and purity of pollen loads for seed set in Rhinanthus angustifolius (Schrophulariaceae) and Viscaria vulgaris (Caryophyllaceae). Oecologia 70:502–507
Le Féon V et al (2010) Intensification of agriculture, landscape composition and wild bee communities: a large scale study in four European countries. Agric Ecosyst Environ 137:143–150
Lentini PE, Martin TG, Gibbons P, Fischer J, Cunningham SA (2012) Supporting wild pollinators in a temperate agricultural landscape: maintaining mosaics of natural features and production. Biol Conserv 149:84–92
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond B 271:2605–2611
Meyer B, Jauker F, Steffan-Dewenter I (2009) Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic Appl Ecol 10:178–186
Milberg P, Persson T (1994) Soil seed bank and species recruitment in road verge grassland vegetation. Ann Bot Fenn 31:155–162
Morandin LA, Abbott VA, Franklin MT (2007) Can pastureland increase wild bee abundance in agriculturally intense areas? Basic Appl Ecol 8:117–124
Mustajärvi K, Siikama P, Åkerberg A (2005) Inbreeding depression in perennial Lychnis viscaria (Caryophyllaceae): effects of population mating history and nutrient availability. Am J Bot 92:1853–1861
Nielsen A, Ims RA (2000) Bumble bee pollination of the sticky catchfly in a fragmented agricultural landscape. Ecoscience 7:157–165
Norderhaug A, Ihse M, Pedersen O (2000) Biotope patterns and abundance of meadow plant species in a Norwegian rural landscape. Landsc Ecol 15:201–218
Öckinger E, Smith HG (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353
Richards AJ (1997) Plant breeding systems. Chapman and Hall, London
Ricketts TH et al (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515
Schmucki R, de Blois ÆS (2009) Pollination and reproduction of a self-incompatible forest herb in hedgerow corridors and forest patches. Oecologia 160:721–733
Schulke B, Waser NM (2001) Long-distance pollinator flights and pollen dispersal between populations of Delphinium nuttallianum. Oecologia 127:239–245
Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440
Steffan-Dewenter I, Munzenberg U, Tscharntke T (2001) Pollination, seed set and seed predation on a landscape scale. Proc R Soc Lond B 268:1685–1690
Steffan-Dewenter Munzenberg U, Burger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432
Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 12:651–652
Steffan-Dewenter I, Klein A-M, Gaebele V, Alfert T, Tscharntke T (2006) Bee diversity and plant-pollinator interactions in fragmented landscapes. In: Waser NM, Ollerton J (eds) Plant-pollinator interaction: from specialization to generalization. University of Chicago Press, Chicago, pp 387–407
Tikka PM, Koski PS, Kivelai RA, Kuitunen MT (2000) Can grassland plant communities be preserved on road and railway verges? Appl Veg Sci 25:25–32
Tommasi D, Miro A, Higo HA, Winston ML (2004) Bee diversity and abundance in an urban setting. Can Entomol 136:851–869
Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216
Vera FWM (2000) Grazing ecology and forest history. CABI Publishing, Wallingford
Waites AR, Ågren J (2004) Pollinator visitation, stigmatic pollen loads and among-population variation in seed set in Lythrum salicaria. J Ecol 92:512–526
Wilson GB, Wright J, Lusby P, Whittington WJ, Humphries RN (1995) Biological flora of the British Isles, no. 188. Lychnis viscaria L. (Viscaria vulgaris Bernh.). J Ecol 83:1039–1051
Wolf AT, Harrison SP (2001) Effects of habitat size and patch isolation on reproductive success of the serpentine morning glory. Conserv Biol 15:111–121
Acknowledgments
Andreas Nyström and Emelie Hedlin provided excellent help in the field. We thank P. Börjesson and J. Ehrlén for statistical advice, and two anonymous reviewers for helpful comments on the manuscript. The study was financed by a grant to A. Jakobsson from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning. The experiments comply with the current laws of Sweden in which the experiments were performed.
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Communicated by Christina Marie Caruso.
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Jakobsson, A., Ågren, J. Distance to semi-natural grassland influences seed production of insect-pollinated herbs. Oecologia 175, 199–208 (2014). https://doi.org/10.1007/s00442-014-2904-z
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DOI: https://doi.org/10.1007/s00442-014-2904-z