Skip to main content

Pollination and reproduction of a self-incompatible forest herb in hedgerow corridors and forest patches

Oecologia volume 160, pages 721–733 (2009)Cite this article

Abstract

Habitat-corridors are assumed to counteract the negative impacts of habitat loss and fragmentation, but their efficiency in doing so depends on the maintenance of ecological processes in corridor conditions. For plants dispersing in linear habitats, one of these critical processes is the maintenance of adequate pollen transfer to insure seed production within the corridor. This study focuses on a common, self-incompatible forest herb, Trillium grandiflorum, to assess plant–pollinator interactions and the influence of spatial processes on plant reproduction in hedgerow corridors compared to forests. First, using pollen supplementation experiments over 2 years, we quantified the extent of pollen limitation in both habitats, testing the prediction of greater limitation in small hedgerow populations than in forests. While pollen limitation of fruit and seed set was common, its magnitude did not differ between habitats. Variations among sites, however, suggested an influence of landscape context on pollination services. Second, we examined the effect of isolation on plant reproduction by monitoring fruit and seed production, as well as pollinator activity and assemblage, in small flower arrays transplanted in hedgerows at increasing distances from forest and from each other. We detected no difference in the proportion of flowers setting fruit or in pollinator activity with isolation, but we observed some differences in pollinator assemblages. Seed set, on the other hand, declined significantly with increasing isolation in the second year of the study, but not in the first year, suggesting altered pollen transfer with distance. Overall, plants in hedgerow corridors and forests benefited from similar pollination services. In this system, plant–pollinator interactions and reproduction seem to be influenced more by variations in resource distribution over years and landscapes than by local habitat conditions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • Adler LS, Irwin RE (2006) Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye. Ann Bot Lond 97:141–150

    PubMed  Article  Google Scholar 

  • Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281

    PubMed  Article  Google Scholar 

  • Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117:1796–1807

    Article  Google Scholar 

  • Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Cox PA, Dalton V, Feinsinger P, Ingram M, Inouye D, Jones CE, Kennedy K, Kevan P, Koopowitz H, Medellin R, Medellin-Morales S, Nabhan GP, Pavlik B, Tepedino V, Torchio P, Walker S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17

    Article  Google Scholar 

  • Artz DR, Waddington KD (2006) The effects of neighbouring tree islands on pollinator density and diversity, and on pollination of a wet prairie species, Asclepias lanceolata (Apocynaceae). J Ecol 94:597–608

    Article  Google Scholar 

  • Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Article  Google Scholar 

  • Bélanger L, Grenier M, Deslandes S, Bossé D (1998) Conservation atlas of woodlands in the agricultural landscape. In: Environment Canada, Canadian Wildlife Service. http://www.qc.ec.gc.ca/faune/atlas/atlas.html

  • Bond WJ (1994) Do mutualisms matter: assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc Lond B 344:83–90

    Article  Google Scholar 

  • Bosch M, Waser NM (1999) Effects of local density on pollination and reproduction in Delphinium nuttallianum and Aconitum columbianum (Ranunculaceae). Am J Bot 86:871–879

    PubMed  Article  Google Scholar 

  • Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126:76–83

    Article  Google Scholar 

  • Brookes RH, Jesson LK, Burd M (2008) A test of simultaneous resource and pollen limitation in Stylidium armeria. New Phytol 179:557–565

    PubMed  Article  Google Scholar 

  • Broyles SB, Shermanbroyles SL, Rogati P (1997) Evidence of outcrossing in Trillium erectum and Trillium grandiflorum (Liliaceae). J Hered 88:325–329

    Google Scholar 

  • Brunet J, Vonoheimb G (1998) Migration of vascular plants to secondary woodlands in southern Sweden. J Ecol 86:429–438

    Article  Google Scholar 

  • Brys R, Jacquemyn H, De Bruyn L, Hermy M (2007) Pollination success and reproductive output in experimental populations of the self-incompatible Primula vulgaris. Int J Plant Sci 168:571–578

    Article  Google Scholar 

  • Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139

    Article  Google Scholar 

  • Burd M (1995) Ovule packaging in stochastic pollination and fertilization environments. Evolution 49:100–109

    Article  Google Scholar 

  • Campbell DR, Halama KJ (1993) Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology 74:1043–1051

    Article  Google Scholar 

  • Case FW, Case RB (1997) Trilliums. Timber Press, Portland

    Google Scholar 

  • Chacoff NP, Aizen MA (2006) Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. J Appl Ecol 43:18–27

    Article  Google Scholar 

  • Colling G, Reckinger C, Matthies D (2004) Effects of pollen quantity and quality on reproduction and offspring vigor in the rare plant Scorzonera humilis (Asteraceae). Am J Bot 91:1774–1782

    Article  Google Scholar 

  • Corbit M, Marks PL, Gardescu S (1999) Hedgerows as habitat corridors for forest herbs in central New York, USA. J Ecol 87:220–232

    Article  Google Scholar 

  • Cranmer L (2004) The influence of linear landscape features on pollinator behaviour. PhD Thesis, University of Northampton, UK

  • Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond Bl 267:1149–1152

    Article  CAS  Google Scholar 

  • de Blois S, Domon G, Bouchard A (2002) Landscape issues in plant ecology. Ecography 25:244–256

    Article  Google Scholar 

  • Duncan DH, Nicotra AB, Wood JT, Cunningham SA (2004) Plant isolation reduces outcross pollen receipt in a partially self-compatible herb. J Ecol 92:977–985

    Article  Google Scholar 

  • Environment Canada (2005) Climate data online. In: Environment Canada. http://climate.weatheroffice.ec.gc.ca

  • Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biol Rev 80:413–443

    PubMed  Article  Google Scholar 

  • Groom MJ (1998) Allee effects limit population viability of an annual plant. Am Nat 151:487–496

    PubMed  Article  CAS  Google Scholar 

  • Haddad NM, Bowne DR, Cunningham A, Danielson BJ, Levey DJ, Sargent S, Spira T (2003) Corridor use by diverse taxa. Ecology 84:609–615

    Article  Google Scholar 

  • Haig D, Westoby M (1988) On limits to seed production. Am Nat 131:757–759

    Article  Google Scholar 

  • Hanzawa FM, Kalisz S (1993) The relationship between age, size, and reproduction in Trillium grandiflorum (Liliaceae). Am J Bot 80:405–410

    Article  Google Scholar 

  • Herrera CM (1995) Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb. Ecology 76:218–228

    Article  Google Scholar 

  • Hines HM, Hendrix SD (2005) Bumble bee (Hymenoptera: Apidae) diversity and abundance in tallgrass prairie patches: effects of local and landscape floral resources. Environ Entomol 34:1477–1484

    Article  Google Scholar 

  • Holzschuh A, Steffan-Dewenter I, Tscharntke T (2008) Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117:354–361

    Article  Google Scholar 

  • Hosmer DWJ, Lemeshow S (2000) Applied logistic regression, 2nd edn. Wiley, New York

    Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Irwin RE (2000) Morphological variation and female reproductive success in two sympatric Trillium species: evidence for phenotypic selection in Trillium erectum and Trillium grandiflorum (Liliaceae). Am J Bot 87:205–214

    PubMed  Article  Google Scholar 

  • Irwin RE (2001) Field and allozyme studies investigating optimal mating success in two sympatric spring-ephemeral plants, Trillium erectum and T. grandiflorum. Heredity 87:178–189

    PubMed  Article  CAS  Google Scholar 

  • Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527

    Article  Google Scholar 

  • Jules ES, Rathcke BJ (1999) Mechanisms of reduced Trillium recruitment along edges of old-growth forest fragments. Conserv Biol 13:784–793

    Article  Google Scholar 

  • Jules ES, Shahani P (2003) A broader ecological context to habitat fragmentation: why matrix habitat is more important than we thought. J Veg Sci 14:459–464

    Article  Google Scholar 

  • Kahmen A, Jules ES (2005) Assessing the recovery of a long-lived herb following logging: Trillium ovatum across a 424-year chronosequence. For Ecol Manag 210:107–116

    Article  Google Scholar 

  • Kalisz S, Hanzawa FM, Tonsor SJ, Thiede DA, Voigt S (1999) Ant-mediated seed dispersal alters pattern of relatedness in a population of Trillium grandiflorum. Ecology 80:2620–2634

    Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Knight TM (2003) Floral density, pollen limitation, and reproductive success in Trillium grandiflorum. Oecologia 137:557–563

    PubMed  Article  Google Scholar 

  • Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman TL (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Evol Syst 36:467–497

    Article  Google Scholar 

  • Knight TM, Steets JA, Ashman TL (2006) A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. Am J Bot 93:271–277

    Article  Google Scholar 

  • Kolb A (2005) Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. J Ecol 93:1226–1237

    Article  Google Scholar 

  • Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vazquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein AM, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314

    PubMed  Article  Google Scholar 

  • Kreyer D, Oed A, Walther-Hellwig K, Frankl R (2004) Are forests potential landscape barriers for foraging bumblebees? Landscape scale experiments with Bombus terrestris agg. and Bombus pascuorum (Hymenoptera, Apidae). Biol Conserv 116:111–118

    Article  Google Scholar 

  • Kunin WE (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. J Ecol 85:225–234

    Article  Google Scholar 

  • Lamont BB, Klinkhamer PGL, Witkowski ETF (1993) Population fragmentation may reduce fertility to zero in Banksia goodii: a demonstration of the Allee effect. Oecologia 94:446–450

    Article  Google Scholar 

  • Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520

    Article  Google Scholar 

  • Lennartsson T (2002) Extinction thresholds and disrupted plant-pollinator interactions in fragmented plant populations. Ecology 83:3060–3072

    Google Scholar 

  • Moody-Weis JM, Heywood JS (2001) Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae). Am J Bot 88:1615–1622

    Article  Google Scholar 

  • Petanidou T, Dennijs JCM, Oostermeijer JGB, Ellisadam AC (1995) Pollination ecology and patch-dependent reproductive success of the rare perennial Gentiana pneumonanthe L. New Phytol 129:155–163

    Article  Google Scholar 

  • Price MV, Waser NM, Irwin RE, Campbell DR, Brody AK (2005) Temporal and spatial variation in pollination of a montane herb: a seven-year study. Ecology 86:2106–2116

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Ricketts T, Imhoff M (2003) Biodiversity, urban areas, and agriculture: locating priority ecoregions for conservation. Conserv Ecol 8:1. http://www.consecol.org/vol8/iss2/art1

  • Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515

    PubMed  Article  Google Scholar 

  • Roy V, de Blois S (2006) Using functional traits to assess the role of hedgerow corridors as environmental filters for forest herbs. Biol Conserv 130:592–603

    Article  Google Scholar 

  • Roy V, de Blois S (2008) Evaluating hedgerow corridors for the conservation of native forest herb diversity. Biol Conserv 141:298–307

    Article  Google Scholar 

  • Sage TL, Griffin SR, Pontieri V, Drobac P, Cole WW, Barrett SCH (2001) Stigmatic self-incompatibility and mating patterns in Trillium grandiflorum and Trillium erectum (Metanthiaceae). Ann Bot Lond 88:829–841

    Article  Google Scholar 

  • SAS Institute (2003) SAS 9.1 for windows. SAS Institute, Cary

    Google Scholar 

  • Saunders DA, Hobbs NT (1991) The role of corridors. Surrey Beatty, London

    Google Scholar 

  • Schmucki R, de Blois S (2009) Population structures and individual performances of Trillium grandiflorum in hedgerow and forest habitats. Plant Ecol 202:67–78. doi:10.1007/s11258-008-9460-8

    Google Scholar 

  • Sih A, Baltus MS (1987) Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology 68:1679–1690

    Article  Google Scholar 

  • Steffan-Dewenter I, Schiele S (2008) Do resources or natural enemies drive bee population dynamics in fragmented habitats? Ecology 89:1375–1387

    PubMed  Article  Google Scholar 

  • Steffan-Dewenter I, Munzenberg U, Burger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432

    Article  Google Scholar 

  • Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652

    PubMed  Article  Google Scholar 

  • Steven JC, Rooney TP, Boyle OD, Waller DM (2003) Density-dependent pollinator visitation and self-incompatibility in upper Great Lakes populations of Trillium grandiflorum. J Torrey Bot Soc 130:23–29

    Article  Google Scholar 

  • Taki H, Kevan PG (2007) Does habitat loss affect the communities of plants and insects equally in plant-pollinator interactions? Preliminary findings. Biodivers Conserv 16:3147–3161

    Article  Google Scholar 

  • Tewksbury JJ, Levey DJ, Haddad NM, Sargent S, Orrock JL, Weldon A, Danielson BJ, Brinkerhoff J, Damschen EI, Townsend P (2002) Corridors affect plants, animals, and their interactions in fragmented landscapes. Proc Natl Acad Sci USA 99:12923–12926

    PubMed  Article  CAS  Google Scholar 

  • Tomimatsu H, Ohara M (2002) Effects of forest fragmentation on seed production of the understory herb Trillium camschatcense. Conserv Biol 16:1277–1285

    Article  Google Scholar 

  • Tomimatsu H, Ohara M (2004) Edge effects on recruitment of Trillium camschatcense in small forest fragments. Biol Conserv 117:509–519

    Article  Google Scholar 

  • Townsend PA, Levey DJ (2005) An experimental test of whether habitat corridors affect pollen transfer. Ecology 86:466–475

    Article  Google Scholar 

  • Wagenius S (2006) Scale dependence of reproductive failure in fragmented Echinacea populations. Ecology 87:931–941

    PubMed  Article  Google Scholar 

  • Wagenius S, Lonsdorf E, Neuhauser C (2007) Patch aging and the S-allee effect: breeding system effects on the demographic response of plants to habitat fragmentation. Am Nat 169:383–397

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Walther-Hellwig K, Frankl R (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., apidae), in an agricultural landscape. J Appl Entomol 124(29):9–306

    Google Scholar 

  • Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59:934–944

    Article  Google Scholar 

  • Waser NM, Price MV (1991) Outcrossing distance effects in Delphinium nelsonii: pollen loads, pollen tubes, and seed set. Ecology 72:171–179

    Article  Google Scholar 

  • Whigham DE (2004) Ecology of woodland herbs in temperate deciduous forests. Annu Rev Ecol Evol Syst 35:583–621

    Article  Google Scholar 

  • Williams NM, Kremen C (2007) Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecol Appl 17:910–921

    PubMed  Article  Google Scholar 

  • Williams NM, Minckley RL, Silveira FA (2001) Variation in native bee faunas and its implications for detecting community changes. Conserv Ecol 5:7

    Google Scholar 

  • Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the Natural Sciences and Engineering Research Council of Canada and the Fonds Québécois de la Recherche sur la Nature et les Technologies. The authors wish to thank B. Gelinas and V. Paul for their assistance with fieldwork and landowners who gave access to their property. We also thank N. Waser and an anonymous reviewer who, with their comments, largely contributed to improve this manuscript. The experiments described here comply with the current laws of Canada and Quebec.

Author information

Authors and Affiliations

  1. Department of Plant Science, Macdonald Campus of McGill University, 21,111 Lakeshore Road, Ste-Anne-de-Bellevue, QC, H9X 3V9, Canada

    Reto Schmucki & Sylvie de Blois

  2. McGill School of Environment, Downtown Campus of McGill University, 3534 University Street, Montreal, QC, H3A 2A7, Canada

    Sylvie de Blois

Authors
  1. Reto Schmucki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sylvie de Blois
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Reto Schmucki.

Additional information

Communicated by Katherine Gross.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary tables (DOC 26 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schmucki, R., de Blois, S. Pollination and reproduction of a self-incompatible forest herb in hedgerow corridors and forest patches. Oecologia 160, 721–733 (2009). https://doi.org/10.1007/s00442-009-1347-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1347-4

Keywords

  • Functional connectivity
  • Habitat corridor
  • Plant–pollinator interaction
  • Pollen limitation
  • Trillium grandiflorum