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.
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References
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
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
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
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
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
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
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
Austerlitz F, Smouse PE (2002) Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161:355–363
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
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
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
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
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
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
Corrick MG, Fuhrer BA (2002) Wildflowers of Western Australia. The Five Miles Press Pty Ltd, Nobel Park
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
Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9
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
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
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
Dixon KW (2009) Pollination and restoration. Science 325:571–573. https://doi.org/10.1126/science.1176295
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13
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
Dyer RJ (2015b) Package ‘gstudio’: tools related to the spatial analysis of genetic marker data, R package version 1.3
Dyer RJ (2015c) Package ‘popgraph’: an R package that constructs and manipulates population graphs, R package version 1.4
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
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
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
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
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
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
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
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
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
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
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
George AS (1981) The Banksia book. Kangaroo Press in association with the Society for Growing Australian Plants, Sydney, NSW
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. v2.9.3. Lausanne University, Lausanne
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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/
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
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
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
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
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
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
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
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
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
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
Suding K et al (2015) Committing to ecological restoration. Science 348:638–640. https://doi.org/10.1126/science.aaa4216
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
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
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
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
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
Wooller R, Wooller SJ (2013) Sugar and Sand: The world of the Honey Possum. Swanbrae Press, Cottesloe
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
Young AG, Clarke GM (eds) (2000) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, UK
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.
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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.
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Communicated by Amy Parachnowitsch.
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.
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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
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DOI: https://doi.org/10.1007/s00442-019-04387-z