Wide outcrossing provides functional connectivity for new and old Banksia populations within a fragmented landscape

Abstract

Habitat fragmentation affects landscape connectivity, the extent of which is influenced by the movement capacity of the vectors of seed and pollen dispersal for plants. Negative impacts of reduced connectivity can include reduced fecundity, increased inbreeding, genetic erosion and decreased long-term viability. These are issues for not only old (remnant) populations, but also new (restored) populations. We assessed reproductive and connective functionality within and among remnant and restored populations of a common tree, Banksia menziesii R.Br. (Proteaceae), in a fragmented urban landscape, utilising a genetic and graph theoretical approach. Adult trees and seed cohorts from five remnants and two restored populations were genotyped using microsatellite markers. Genetic variation and pollen dispersal were assessed using direct (paternity assignment) and indirect (pollination graphs and mating system characterisation) methods. Restored populations had greater allelic diversity (Ar = 8.08; 8.34) than remnant populations (Ar range = 6.49–7.41). Genetic differentiation was greater between restored and adjacent remnants (FST = 0.03 and 0.10) than all other pairwise comparisons of remnant populations (mean FST = 0.01 ± 0.01; n = 16 P = 0.001). All populations displayed low correlated paternity (rp = 0.06–0.16) with wide-ranging realised pollen dispersal distances (< 1.7 km) and well-connected pollen networks. Here, we demonstrate reproductive and connective functionality of old and new populations of B. menziesii within a fragmented landscape. Due to long-distance pollination events, the physical size of these sites underestimates their effective population size. Thus, they are functionally equivalent to large populations, integrated into a larger landscape matrix.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aavik T, Helm A (2017) Restoration of plant species and genetic diversity depends on landscape-scale dispersal. Restor Ecol. https://doi.org/10.1111/rec.12634

    Article  Google Scholar 

  2. Aavik T, Holderegger R, Edwards PJ, Billeter R (2013) Patterns of contemporary gene flow suggest low functional connectivity of grasslands in a fragmented agricultural landscape. J Appl Ecol 50:395–403. https://doi.org/10.1111/1365-2664.12053

    Article  Google Scholar 

  3. Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through meta-analysis. Ecol Lett 9:968–980. https://doi.org/10.1111/j.1461-0248.2006.00927.x

    Article  PubMed  Google Scholar 

  4. Aizen MA, Gleiser G, Sabatino M, Gilarranz LJ, Bascompte J, Verdú M (2016) The phylogenetic structure of plant–pollinator networks increases with habitat size and isolation. Ecol Lett 19:29–36. https://doi.org/10.1111/ele.12539

    Article  PubMed  Google Scholar 

  5. Auffret AG, Rico Y, Bullock JM et al (2017) Plant functional connectivity—integrating landscape sructure and effective dispersal. J Ecol 105:1648–1656. https://doi.org/10.1111/1365-2745.12742

    Article  Google Scholar 

  6. Austerlitz F, Smouse PE (2001a) Two-generation analysis of pollen flow across a landscape III. Impact of adult population structure. Genet Res Camb 78:271–280. https://doi.org/10.1017/S0016672301005341

    Article  CAS  Google Scholar 

  7. Austerlitz F, Smouse PE (2001b) Two-generation analysis of pollen flow across a landscape. II. Relation between Фft, pollen dispersal and interfemale distance. Genetics 157:851–857

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Austerlitz F, Smouse PE (2002) Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161:355–363

    PubMed  PubMed Central  Google Scholar 

  9. Baker SA, Dyer RJ (2011) Invasion genetics of Microstegium vimineum (Poaceae) within the James River Basin of Virginia, USA. Cons Gen 12:793–803. https://doi.org/10.1007/s10592-011-0186-0

    Article  Google Scholar 

  10. Breed MF, Ottewell KM, Gardner MG, Marklund MH, Stead MG, Harris JB, Lowe AJ (2015) Mating system and early viability resistance to habitat fragmentation in a bird-pollinated eucalypt. Heredity 115:100–107. https://doi.org/10.1038/hdy.2012.72

    Article  CAS  PubMed  Google Scholar 

  11. Byrne M, Elliott C, Yates C, Coates D (2007) Extensive pollen dispersal in a bird-pollinated shrub, Calothamnus quadrifidus, in a fragmented landscape. Mol Ecol 16:1303–1314. https://doi.org/10.1111/j.1365-294X.2006.03204.x

    Article  CAS  PubMed  Google Scholar 

  12. Byrne M, Elliott CP, Yates CJ, Coates DJ (2008) Maintenance of high pollen dispersal in Eucalyptus wandoo, a dominant tree of the fragmented agricultural region in Western Australia. Conserv Genet 9:97–105. https://doi.org/10.1007/s10592-007-9311-5

    Article  Google Scholar 

  13. Coates DJ, Sampson JF, Yates CJ (2007) Plant mating systems and assessing population persistence in fragmented landscapes. Aust J Bot 55:239. https://doi.org/10.1071/BT06142

    Article  Google Scholar 

  14. Comer SJ, Wooller RD (2002) A comparison of the passerine avifaunas of rehabilitated minesite and nearby reserve in south-western Australia. Emu 102:305–311. https://doi.org/10.1071/MU00042

    Article  Google Scholar 

  15. Corrick MG, Fuhrer BA (2002) Wildflowers of Western Australia. The Five Miles Press Pty Ltd, Nobel Park

    Google Scholar 

  16. Crouzeilles R, Curran M (2016) Which landscape size best predicts the influence of forest cover on restoration success? A global meta-analysis on the scale of effect. J Appl Ecol 53:440–448. https://doi.org/10.1111/1365-2664.12590

    Article  Google Scholar 

  17. Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9

    Google Scholar 

  18. Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond B 267:1149–1152. https://doi.org/10.1098/rspb.2000.1121

    Article  CAS  Google Scholar 

  19. Davis RA, Wilcox J (2013) Adapting to suburbia: bird ecology on an urban-bushland interface in Perth, Western Australia. Pac Conserv Biol 19:110–120. https://doi.org/10.1071/PC130110

    Article  Google Scholar 

  20. Davis RA, Gole C, Roberts JD (2013) Impacts of urbanisation on the native avifauna of Perth, Western Australia. Urban Ecosys 16:427–452. https://doi.org/10.1007/s11252-012-0275-y

    Article  Google Scholar 

  21. Dixon KW (2009) Pollination and restoration. Science 325:571–573. https://doi.org/10.1126/science.1176295

    Article  CAS  PubMed  Google Scholar 

  22. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13

    Google Scholar 

  23. Dyer RJ (2015a) Population graphs and landscape genetics. Annu Rev Ecol Evol Syst 46:327–342. https://doi.org/10.1146/annurev-ecolsys-112414-054150

    Article  Google Scholar 

  24. Dyer RJ (2015b) Package ‘gstudio’: tools related to the spatial analysis of genetic marker data, R package version 1.3

  25. Dyer RJ (2015c) Package ‘popgraph’: an R package that constructs and manipulates population graphs, R package version 1.4

  26. Dyer RJ, Nason JD (2004) Population Graphs: the graph theoretic shape of genetic structure. Mol Ecol 13:1713–1727. https://doi.org/10.1111/j.1365-294X.2004.02177.x

    Article  PubMed  Google Scholar 

  27. Dyer RJ, Sork VL (2001) Pollen Pool Heterogeneity in Shortleaf Pine, Pinus echinata Mill. Mol Ecol 10:859–866. https://doi.org/10.1046/j.1365-294X.2001.01251.x

    Article  CAS  PubMed  Google Scholar 

  28. Dyer RJ, Nason JD, Garrick RC (2010) Landscape modeling of gene flow: improved power using conditional genetic distance derived from the topology of population networks. Mol Ecol 19:3746–3759. https://doi.org/10.1111/j.1365-294X.2010.04748.x

    Article  PubMed  Google Scholar 

  29. Dyer RJ, Chan DM, Gardiakos VA, Meadows CA (2012) Pollination graphs: quantifying pollen pool covariance networks and the influence of intervening landscape on genetic connectivity in the North American understory tree, Cornus florida L. Landsc Ecol 27:239–251. https://doi.org/10.1007/s10980-011-9696-x

    Article  Google Scholar 

  30. Eckert CG, Kalisz S, Geber MA et al (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43. https://doi.org/10.1016/j.tree.2009.06.013

    Article  PubMed  Google Scholar 

  31. Elliott C, Lindenmayer D, Cunningham S, Young A (2012) Landscape context affects honeyeater communities and their foraging behaviour in Australia: implications for plant pollination. Lands Ecol 27:393–404. https://doi.org/10.1007/s10980-011-9697-9

    Article  Google Scholar 

  32. Forup ML, Memmott J (2005) The restoration of plant–pollinator interactions in hay meadows. Restor Ecol 13:265–274. https://doi.org/10.1111/j.1526-100X.2005.00034.x

    Article  Google Scholar 

  33. Forup ML, Henson KSE, Craze PG, Memmott J (2008) The restoration of ecological interactions: plant–pollinator networks on ancient and restored heathlands. J Appl Ecol 45:742–752. https://doi.org/10.1111/j.1365-2664.2007.01390.x

    Article  Google Scholar 

  34. Frankham R, Ballou JD, Eldridge MDB et al (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475. https://doi.org/10.1111/j.1523-1739.2011.01662.x

    Article  PubMed  Google Scholar 

  35. Frick KM, Ritchie AL, Krauss SL (2014) Field of dreams: restitution of pollinator services in restored bird-pollinated plant populations. Restor Ecol 22:832–840. https://doi.org/10.1111/rec.12152

    Article  Google Scholar 

  36. Garrick RC, Nason JD, Meadows CA, Dyer RJ (2009) Not just vicariance: phylogeography of a Sonoran desert euphorb indicates a major role of range expansion along the Baja peninsula. Mol Ecol 18:1916–1931. https://doi.org/10.1111/j.1365-294X.2009.04148.x

    Article  CAS  PubMed  Google Scholar 

  37. George AS (1981) The Banksia book. Kangaroo Press in association with the Society for Growing Australian Plants, Sydney, NSW

    Google Scholar 

  38. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. v2.9.3. Lausanne University, Lausanne

    Google Scholar 

  39. He T, Krauss SL, Lamont BB, Miller BP, Enright NJ (2004) Long-distance seed dispersal in a metapopulation of Banksia hookeriana inferred from a population allocation analysis of amplified fragment length polymorphism data. Mol Ecol 13:1099–1109. https://doi.org/10.1111/j.1365-294X.2004.02120.x

    Article  CAS  PubMed  Google Scholar 

  40. He T, Krauss S, Lamont BB (2007) Polymorphic microsatellite DNA markers for Banksia attenuata (Proteaceae). Mol Ecol Notes 7:1329–1331. https://doi.org/10.1111/j.1471-8286.2007.01871.x

    Article  CAS  Google Scholar 

  41. Heliyanto B, Krauss SL, Lambers H, Cawthray GR, Veneklaas EJ (2006) Increased ecological amplitude through heterosis following wide outcrossing in Banksia ilicifolia R.Br. (Proteaceae). J Evol Biol 19:1327–1338. https://doi.org/10.1111/j.1420-9101.2005.01067.x

    Article  CAS  PubMed  Google Scholar 

  42. Helsen K, Jacquemyn H, Hermy M, Vandepitte K, Honnay O (2013) Rapid buildup of genetic diversity in founder populations of the Gynodioecious plant species Origanum vulgare after semi-natural grassland restoration. PLoS ONE 8:e67255. https://doi.org/10.1371/journal.pone.0067255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometric J 50:346–363. https://doi.org/10.1002/bimj.200810425

    Article  Google Scholar 

  44. Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155. https://doi.org/10.1016/S0169-5347(03)00002-8

    Article  Google Scholar 

  45. Jobes DV, Hurley DL, Thien LB (1995) Plant DNA isolation: a method to efficiently remove polyphenolics, polysaccharides, and RNA. Taxon 1:379–386. https://doi.org/10.2307/1223408

    Article  Google Scholar 

  46. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol Notes 16:1099–1106. https://doi.org/10.1111/j.1365-294X.2007.03089.x

    Article  Google Scholar 

  47. Kettenring KM, Mercer KL, Reinhardt Adams C, Hines J (2014) Application of genetic diversity–ecosystem function research to ecological restoration. J Appl Ecol 51:339–348. https://doi.org/10.1111/1365-2664.12202

    Article  Google Scholar 

  48. Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conserv Biol 22:878–885. https://doi.org/10.1111/j.1523-1739.2008.00944.x

    Article  PubMed  Google Scholar 

  49. Krauss SL, He T, Barrett LG, Lamont BB, Enright NJ, Miller BP, Hanley ME (2009) Contrasting impacts of pollen and seed dispersal on spatial genetic structure in the bird-pollinated Banksia hookeriana. Heredity 102:274–285. https://doi.org/10.1038/hdy.2008.118

    Article  CAS  PubMed  Google Scholar 

  50. Krauss SL, Sinclair EA, Bussell JD, Hobbs RJ (2013) An ecological genetic delineation of local seed-source provenance for ecological restoration. Ecol Evol 3:2138–2149. https://doi.org/10.1002/ece3.595

    Article  PubMed  PubMed Central  Google Scholar 

  51. Krauss SL, Phillips RD, Karron JD, Johnson SD, Roberts DG, Hopper SD (2017) Novel consequences of bird pollination for plant mating. Trends Plant Sci 2:395–410. https://doi.org/10.1016/j.tplants.2017.03.005

    Article  CAS  Google Scholar 

  52. 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. https://doi.org/10.1007/BF00317122

    Article  PubMed  Google Scholar 

  53. Lamont BB, Enright NJ, Witkowski ETF, Groeneveld J (2007) Conservation biology of banksias: insights from natural history to simulation modelling. Aust J Bot 55:280–292. https://doi.org/10.1071/BT06024

    Article  Google Scholar 

  54. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655. https://doi.org/10.1046/j.1365-294x.1998.00374.x

    Article  CAS  PubMed  Google Scholar 

  55. McKay JK, Christian CE, Harrison S, Rice KJ (2005) “How local is local?”—A review of practical and conceptual issues in the genetics of restoration. Restor Ecol 13:432–440. https://doi.org/10.1111/j.1526-100X.2005.00058.x

    Article  Google Scholar 

  56. Menz MH, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16:4–12. https://doi.org/10.1016/j.tplants.2010.09.006

    Article  CAS  PubMed  Google Scholar 

  57. Menz MH, Dixon KW, Hobbs RJ (2013) Hurdles and opportunites for landscape-scale restoration. Science 339:526–527. https://doi.org/10.1126/science.1228334

    Article  CAS  PubMed  Google Scholar 

  58. Mijangos JL, Pacioni C, Spencer P, Craig MD (2015) Contribution of genetics to ecological restoration. Mol Ecol 24:22–37. https://doi.org/10.1111/mec.12995

    Article  PubMed  Google Scholar 

  59. Miller BP et al (2017) A framework for the practical science necessary to restore sustainable, resilient, and biodiverse ecosystems. Restor Ecol 25:605–617. https://doi.org/10.1111/rec.12475

    Article  Google Scholar 

  60. Munro NT, Fischer J, Barrett G, Wood J, Leavesley A, Lindenmayer DB (2011) Bird’s response to revegetation of different structure and floristics – are “restoration plantings” restoring bird communities? Restor Ecol 19:223–235. https://doi.org/10.1111/j.1526-100X.2010.00703.x

    Article  Google Scholar 

  61. Newland CE, Wooller RD (1985) Seasonal changes in a honeyeater assemblage in Banksia woodland near Perth, Western Australia. N.Z. J Zool 12:631–636. https://doi.org/10.1080/03014223.1985.10428312

    Article  Google Scholar 

  62. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x

    Article  Google Scholar 

  63. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Perring MP, Standish RJ, Price JN, Craig MD, Erickson TE, Ruthrof KX, Whiteley AS, Valentine LE, Hobbs RJ (2015) Advances in restoration ecology: rising to the challenges of the coming decades. Ecosphere 6:1–25. https://doi.org/10.1890/ES15-00121.1

    Article  Google Scholar 

  65. Proft KM, Jones ME, Johnson CN, Burridge CP (2018) Making the connection: expanding the role of restoration genetics in restoring and evaluating connectivity. Restor Ecol 1:1. https://doi.org/10.1111/rec.12692

    Article  Google Scholar 

  66. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN: 3-900051-900007-900050. http://www.R-project.org/

  67. Ramsay MW (1988) Differences in pollinator effectiveness of birds and insects visiting Banksia menziesii (Proteaceae). Oecologia 76:119–124. https://doi.org/10.1007/BF00379609

    Article  Google Scholar 

  68. Ramsay MW (1989) The seasonal abundance and foraging behaviour of honeyeaters and their potential role in the pollination of Banksia menziesii. Aust J Ecol 14:33–40. https://doi.org/10.1111/j.1442-9993.1989.tb01006.x

    Article  Google Scholar 

  69. Ritchie AL, Krauss SL (2012) A genetic assessment of ecological restoration success in Banksia attenuata. Restor Ecol 20:441–449. https://doi.org/10.1111/j.1526-100X.2011.00791.x

    Article  Google Scholar 

  70. Ritchie A, Nevill PG, Sinclair EA, Krauss SL (2017) Does restored plant diversity play a role in the reproductive functionality of Banksia populations? Restor Ecol 25:414–423. https://doi.org/10.1111/rec.12456

    Article  Google Scholar 

  71. Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228. https://doi.org/10.1038/sj.hdy.6800029

    Article  PubMed  Google Scholar 

  72. Scott JK (1980) Estimation of the outcrossing rate for Banksia attenuata R.Br. and Banksia menziesii R.Br. (Proteaceae). Aust J Bot 28:53–59. https://doi.org/10.1071/BT9800053

    Article  Google Scholar 

  73. Shanahan DF, Miller C, Possingham HP, Fuller RA (2011) The influence of patch area and connectivity on avian comunities in urban revegetation. Biol Cons 144:722–729. https://doi.org/10.1016/j.biocon.2010.10.014

    Article  Google Scholar 

  74. Slate J, Marshall T, Pemberton J (2000) A retrospective assessmnet of the accuracy of the paternity inference program CERVUS. Mol Ecol 9:801–808. https://doi.org/10.1046/j.1365-294x.2000.00930.x

    Article  CAS  PubMed  Google Scholar 

  75. Smouse PE, Dyer RJ, Westfall RD, Sork VL (2001) Two-generation analysis of pollen flow across a landscape I. male gamete heterogeneity among females. Evolution 55:260–271. https://doi.org/10.1554/0014-3820(2001)055%5b0260:TGAOPF%5d2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  76. Stevens JC, Rokich DP, Newton VJ, Barrett RL, Dixon KW (2016) Banksia woodlands: A restoration guide for the Swan Coastal Plain. UWA Press, Western Australia

    Google Scholar 

  77. Suding K et al (2015) Committing to ecological restoration. Science 348:638–640. https://doi.org/10.1126/science.aaa4216

    Article  CAS  PubMed  Google Scholar 

  78. Thomas E, Jalonen R, Loo J, Boshier D, Gallo L, Cavers S, Bordács S, Smith P, Bozzano M (2014) Genetic considerations in ecosystem restoration using native tree species. For Ecol Manage 333:66–75. https://doi.org/10.1016/j.foreco.2014.07.015

    Article  Google Scholar 

  79. Tulloch AIT, Barnes MD, Ringma J, Fuller RA, Watson JEM (2015) Understanding the importance of small patches of habitat for conservation. J Appl Ecol 53:418–429. https://doi.org/10.1111/1365-2664.12547

    Article  Google Scholar 

  80. Valiente-Banuet A et al (2015) Beyond species loss: the extinction of ecological interactions in a changing world. Funct Ecol 29:299–307. https://doi.org/10.1111/1365-2435.12356

    Article  Google Scholar 

  81. Vranckx G, Jacquemyn H, Muys B, Honnay O (2012) Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv Biol 26:228–237. https://doi.org/10.1111/j.1523-1739.2011.01778.x

    Article  PubMed  Google Scholar 

  82. Williams AV, Nevill PG, Krauss SL (2014) Next generation restoration genetics: applications and opportunities. Trends Plant Sci 19:529–537. https://doi.org/10.1016/j.tplants.2014.03.011

    Article  CAS  PubMed  Google Scholar 

  83. Wooller R, Wooller SJ (2013) Sugar and Sand: The world of the Honey Possum. Swanbrae Press, Cottesloe

    Google Scholar 

  84. Wortley L, Hero J-M, Howes M (2013) Evaluating ecological restoration success: a review of the literature. Rest Ecol 21:537–543. https://doi.org/10.1111/rec.12028

    Article  Google Scholar 

  85. Young AG, Clarke GM (eds) (2000) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, UK

    Google Scholar 

Download references

Acknowledgements

Thanks to Janet Anthony for assistance with the genetic work undertaken in the laboratory and Carole Elliott and Bryn Funnekotter for providing comments and helpful suggestions for improving the paper. This work was supported by Rocla Quarry Products (now Hanson Construction Materials), a Holsworth Wildlife Research Endowment and a Friends of Kings Park writing scholarship to ALR, the Botanic Gardens and Parks Authority and a linkage grant to SLK from the Australian Research Council (LP100100620). ALR was supported by an Australian Postgraduate Award during this study.

Author information

Affiliations

Authors

Contributions

ALR, PGN, EAS and SLK conceived and designed the research. ALR performed the study and analysed the data. Popgraph analysis was performed by ALR and RJD. All authors contributed to writing the manuscript.

Corresponding author

Correspondence to Alison L. Ritchie.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

This study is one of the first to examine plant functional connectivity, measuring effective pollen dispersal using new methods in landscape genetics. We found that new populations have integrated with old through long-distance pollination events. Retaining remnant populations in the urban matrix is vital for maintaining reproductive functionality at the landscape scale.

Communicated by Amy Parachnowitsch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 163 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ritchie, A.L., Dyer, R.J., Nevill, P.G. et al. Wide outcrossing provides functional connectivity for new and old Banksia populations within a fragmented landscape. Oecologia 190, 255–268 (2019). https://doi.org/10.1007/s00442-019-04387-z

Download citation

Keywords

  • Banksia menziesii
  • Restoration
  • Mating system
  • Pollinator services
  • Popgraph