Skip to main content

Advertisement

SpringerLink
Log in

Conservation by translocation: establishment of Wollemi pine and associated microbial communities in novel environments

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Wollemi pine (Wollemia nobilis Jones, Hill & Allen) is a critically endangered conifer and living fossil. Translocation has been proposed as a conservation strategy to establish ‘back-ups’ to the wild population; however, knowledge regarding the environmental and biotic requirements of individuals planted in new environments is limited.

Methods

An experimental translocation was established in a new location in the wild with Wollemi pines planted along a light and elevation gradient. Specific abiotic soil properties and associated microbial communities were linked to Wollemi pine performance in these new locations to inform best practice for future translocations.

Results

Our results indicate that soil properties can be used to select appropriate translocation sites that ensure initial establishment and growth. One year after translocation Wollemi pine had recruited a species-specific fungal community that persisted. Species-specific bacterial communities in their soil and roots formed in the second year after planting. Translocated Wollemi pines that were unhealthy and were not growing did not have the species-specific fungal community.

Conclusion

The long-term functional consequence of this species-specific microbial community warrants ongoing investigation. This is one of the first studies to explicitly consider the role of microbial communities during the translocation of a rare plant and such approaches will be valuable for informing best translocation practice for other rare plant species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdo Z, Schüette U, Bent S, et al. (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938. doi:10.1111/j.1462-2920.2005.00959.x

    Article  PubMed  Google Scholar 

  • Abeli T, Dixon K (2016) Translocation ecology: the role of ecological sciences in plant translocation. Plant Ecol editorial:1–3. doi:10.1007/s11258-016-0575-z

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. doi:10.1007/s005720100097

    Article  Google Scholar 

  • Augé R, Toler H, Saxton A (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24. doi:10.1007/s00572-014-0585-4

    Article  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, et al. (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, et al. (2015) Fitting Linear Mixed-Effects Models Using. J Stat Softw 67(1)

  • Benson J, Allen C (2007) Vegetation associated with Wollemia nobilis (Araucariaceae). Cunninghamia 10:255–262

    Google Scholar 

  • Bever J (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977

    Article  Google Scholar 

  • Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bieleski R (1959) Factors affecting growth and distribution of kauri (Agathis australis Salisb.) III. Effect of temperature and soil conditions. Aust J Bot 7:279. doi:10.1071/BT9590279

    Article  Google Scholar 

  • Biggs, L (2009) Mycorrhizal inoculation, endophytic colonization, and allelopathic potential of the Wollemi pine (Wollemia nobilis). Masters Thesis, The University of British Columbia.

  • Bonanomi G, Giannino F, Mazzoleni S (2005) Negative plant–soil feedback and species coexistence. Oikos 111:311–321. doi:10.1111/j.0030-1299.2005.13975.x

    Article  Google Scholar 

  • Bray R, Kurtz L (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46

  • Chemidlin Prévost-Bouré N, Dequiedt S, Thioulouse J, et al. (2014) Similar processes but different environmental filters for soil bacterial and fungal community composition turnover on a broad spatial scale. PLoS One 9:e111667. doi:10.1371/journal.pone.0111667

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark D, Clark DB (1984) Spacing dynamics of a tropical rain forest tree: evaluation of the Janzen-Connell model. Am Nat 124:769–788

    Article  Google Scholar 

  • Connell J (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rainforest trees. In: Boer D, Gradwell G (eds) Dynamics of Populations- Proceedings of the Advanced Study Institute. Centre for Agricultural Publishing and Documentation, Wageningen, pp. 298–312

    Google Scholar 

  • Culman SW, Bukowski R, Gauch HG, et al (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10:171.

  • Curlevski NJA, Xu Z, Anderson IC, Cairney JWG (2010) Converting Australian tropical rainforest to native Araucariaceae plantations alters soil fungal communities. Soil Biol Biochem 42:14–20. doi:10.1016/j.soilbio.2009.08.001

    Article  CAS  Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Found. Stat. Comput

  • Donaldson JS (2009) Botanic gardens science for conservation and global change. Trends Plant Sci 14:608–613. doi:10.1016/j.tplants.2009.08.008

    Article  CAS  PubMed  Google Scholar 

  • Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115. doi:10.1146/annurev.energy.30.050504.144212

    Article  Google Scholar 

  • Eviner VT, Hawkes CV (2008) Embracing variability in the application of plant-soil interactions to the restoration of communities and ecosystems. Restor Ecol 16:713–729. doi:10.1111/j.1526-100X.2008.00482.x

    Article  Google Scholar 

  • Fox J, Weisberg S (2011) An R Companion to Applied Regression, 2nd edn. Thousand Oaks, California

    Google Scholar 

  • Gardes M, Bruns T (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  PubMed  Google Scholar 

  • Godefroid S, Piazza C, Rossi G, et al. (2011) How successful are plant species reintroductions? Biol Conserv 144:672–682. doi:10.1016/j.biocon.2010.10.003

    Article  Google Scholar 

  • Gordon D (1996) Experimental translocation of the endangered shrub Apalachicola rosemary Conradina glabra to the Apalachicola bluffs and ravines preserve, Florida. Biol Conserv 77:19–26

    Article  Google Scholar 

  • Gosling P, Jones J, Bending GD (2016) Evidence for functional redundancy in arbuscular mycorrhizal fungi and implications for agroecosystem management. Mycorrhiza 26:77–83. doi:10.1007/s00572-015-0651-6

    Article  PubMed  Google Scholar 

  • Guerrant EO, Kaye TN (2007) Reintroduction of rare and endangered plants: common factors, questions and approaches. Aust J Bot 55:362–370

    Article  Google Scholar 

  • Handreck K, Black N (1999) Growing media for ornamental plants and turfs. University of New South Wales Press, Sydney

    Google Scholar 

  • Harris J (2009) Soil microbial communities and restoration ecology: facilitators or followers? Science 325(80-):573–574. doi:10.1126/science.1172975

    Article  CAS  PubMed  Google Scholar 

  • Hauben L, Vauterin L, Swings J, Moore E (1997) Comparison of 16S ribosomal DNA sequence of all Xanthomonas species. Int J Syst Evol Microbiol 47:328–335

    CAS  Google Scholar 

  • Janzen D (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:592–595

    Article  Google Scholar 

  • Jasper DA (2007) Beneficial soil microorganisms of the Jarrah forest and their recovery in bauxite mine restoration in southwestern Australia. Restor Ecol 15:74–84. doi:10.1111/j.1526-100X.2007.00295.x

    Article  Google Scholar 

  • Jusaitis M, Polomka L, Sorensen B (2004) Habitat specificity, seed germination and experimental translocation of the endangered herb. Brachycome muelleri (Asteraceae) 116(2):251–266

  • Kaye TN (2008) Vital steps toward success of endangered plant reintroductions. Nativ Plants J 9:313–322

    Article  Google Scholar 

  • Klironomos J (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  CAS  PubMed  Google Scholar 

  • Lankau RA (2013) Species invasion alters local adaptation to soil communities in a native plant. Ecology 94:32–40. doi:10.1890/12-0675.1

    Article  PubMed  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. doi:10.1128/AEM.00335-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Liu X, Ellsworth DS, Tyree MT (1997) Leaf nutrition and photosynthetic performance of sugar maple (Acer saccharum) in stands with contrasting health conditions. Tree Physiol 17:169–178. doi:10.1093/treephys/17.3.169

    Article  CAS  PubMed  Google Scholar 

  • Mangan SA, Schnitzer SA, Herre EA, et al (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. doi: http://www.nature.com/nature/journal/v466/n7307/abs/nature09273.html#supplementary-information.

  • Marchesi J, Sato T, Weightman A, et al. (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    CAS  PubMed  PubMed Central  Google Scholar 

  • McGee P, Bullock S, Summerell B (1999) Structure of mycorrhizae of the Wollemi pine (Wollemia noblis) and related Araucariaceae. Aust J Bot 47:5–95

    Article  Google Scholar 

  • Menges ES (2008) Turner review no. 16. Restoration demography and genetics of plants: when is a translocation successful? Aust J Bot 56:187–196

    Article  Google Scholar 

  • Middleton EL, Bever JD (2012) Inoculation with a native soil community advances succession in a grassland restoration. Restor Ecol 20:218–226. doi:10.1111/j.1526-100X.2010.00752.x

    Article  Google Scholar 

  • Monks L, Coates D, Bell T, Bowles M (2012) Determining success criteria for reintroductions of threatened long-lived plants. In: Plant reintroduction in a changing climate: promises and perils Island Press, Washington DC

  • Murphy CA, Foster BL (2014) Soil properties and spatial processes influence bacterial Metacommunities within a grassland restoration experiment. Restor Ecol 22:685–691. doi:10.1111/rec.12127

    Article  Google Scholar 

  • NSW Department of Environment and Conservation (2006) Wollemi Pine (Wollemia nobilis) Recovery Plan. NSW Department of Environment and Conservation, Hurstville, pp. 1–37

  • Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359

    Article  PubMed  Google Scholar 

  • Offord C, Porter C, Meagher P, Errington G (1999) Sexual reproduction and early plant growth of the Wollemi pine (Wollemia nobilis) a rare and threatened Australian conifer. Ann Bot 84:1–9

    Article  Google Scholar 

  • Offord CA, Meagher PF, Zimmer HC (2014) Growing up or growing out? How soil pH and light affect seedling growth of a relictual rainforest tree. AoB. Plants 6:plu011. doi:10.1093/aobpla/plu011

    Google Scholar 

  • Oksanen J, Blanchet F, Kindt R, et al (2007) vegan: community ecology package. R Packag. http://www.CRAN.R-project.org/package=vegan

  • Plassart P, Akpa Vinceslas M, Gangneux C, et al. (2008) Molecular and functional responses of soil microbial communities under grassland restoration. Agric Ecosyst Environ 127:286–293. doi:10.1016/j.agee.2008.04.008

    Article  CAS  Google Scholar 

  • Potthoff M, Steenwerth KL, Jackson LE, et al. (2006) Soil microbial community composition as affected by restoration practices in California grassland. Soil Biol Biochem 38:1851–1860. doi:10.1016/j.soilbio.2005.12.009

    Article  CAS  Google Scholar 

  • Powell JR, Bennett AE (2015) Unpredictable assembly of arbuscular mycorrhizal fungal communities. Pedobiologia (Jena) 59:11–15. doi:10.1016/j.pedobi.2015.12.001

    Article  Google Scholar 

  • Powell JR, Karunaratne S, Campbell CD, et al. (2015) Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat Commun 6:1–10

    Article  CAS  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, et al. (2000) Plant invasions — the role of mutualisms. Biol Rev 75:65–93. doi:10.1111/j.1469-185X.1999.tb00041.x

    Article  CAS  PubMed  Google Scholar 

  • Rigg J, Offord C, BK S, et al. (2016a) Variation in soil microbial communities associated with critically endangered Wollemi pine affects fungal, but not bacterial, assembly within seedling roots. Pedobiologia (Jena) 59:61–71. doi:10.1016/j.pedobi.2016.02.002

    Article  Google Scholar 

  • Rigg J, (2016b) Microbial influences on the conservation and recovery of wollemi pine. PhD Thesis. Western Sydney University (in press)

  • Rillig MC, Antonovics J, Caruso T, et al. (2015) Interchange of entire communities: microbial community coalescence. Trends Ecol Evol 30:470–476. doi:10.1016/j.tree.2015.06.004

  • Rillig MC, Lehmann A, Aguilar-Trigueros C, et al. (2016) Soil microbes and community coalescence. Pedobiologia (Jena) 59:37–40. doi:10.1016/j.pedobi.2016.01.001

    Article  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, et al. (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi:10.1038/ismej.2010.58

    Article  PubMed  Google Scholar 

  • Seal Analytic (2011) Method Number: EPA-118_A Rev. 5: o-Phosphate-P in drinking, saline and surface waters, and domestic and industrial wastes. http://www.seal-analytical.com/Methods/DiscreteMethods/AQ2EPAMethods/tabid/76/language/en-US/Default.aspx.

  • Silvester WB, Orchard TA (1999) The biology of kauri ( Agathis australis ) in New Zealand. Production, biomass, carbon storage, and litter fall in four forest remnants. New zeal. J Bot 37:553–571. doi:10.1080/0028825X.1999.9512653

    Google Scholar 

  • Singh B, Nazaries L, Munro S, et al. (2006) Use of multiplex terminal restriction fragment length polymorphism for rapid and simultaneous analysis of different components of the soil microbial community. Appl Environ Microbiol 72:7278–7285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (1997) Chapter 17: Mycorrhizas in managed environments: Forest production, interactions with other microorganisms and pollutants. In: Mycorrhizal Symbiosis (Second Edition). Academic Press, London, pp 470–489

  • Smith C, Danilowicz B, Clear A, et al. (2005) T-align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol Ecol 54:375–380. doi:10.1016/j.femsec.2005.05.002

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Bahram M, Polme S, et al. (2014) Global diversity and geography of soil fungi. Science 346(80-):1256688–1256688. doi:10.1126/science.1256688

    Article  PubMed  Google Scholar 

  • Thomas P (2011) The IUCN Red List of Threatened Species 2011: e.T34926 A9898196. www.iucnredlist.org. Accessed 29 Mar 2016

  • Vallee L, Hogbin T, Monks L, et al. (2004) Guidelines for the translocation of threatened plants in Australia, 2nd Editio. Australian Network for Plant Conservation, Canberra

    Google Scholar 

  • Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1:15159. doi:10.1038/nplants.2015.159

    Article  CAS  PubMed  Google Scholar 

  • White B, Taylor DL (1990) Analysis of phylogenetic relationship by amplification and direct sequencing of ribosomal RNA genes. In: PCR protocol: a guide to method and applications Academic Press, New York, pp 315–322

  • Wyse S (2012) Growth responses of five forest plant species to the soils formed beneath New Zealand kauri (Agathis australis). New zeal. J Bot 50:411–421. doi:10.1080/0028825X.2012.724428

    Google Scholar 

  • Yang C-H, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66:345–351. doi:10.1128/AEM.66.1.345-351.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer HC, Offord CA, Auld TD, Baker PJ (2016) Establishing a wild, ex situ population of a critically endangered shade-tolerant rainforest conifer: a translocation experiment. PLoS One 11:e0157559. doi:10.1371/journal.pone.0157559

    Article  PubMed  PubMed Central  Google Scholar 

  • Zoë FS, Elizabeth AJ, Mark JM, Cassandra BM (2009) Planting conditions improve translocation success of the endangered terrestrial orchid Diuris fragrantissima (Orchidaceae. Aust J Bot 57:200–209. doi:10.1071/BT09072

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Tony Auld and the Wollemi pine recovery team for their approval to conduct the experimental translocation and approval to use plants from the ex situ collection of Wollemi pine. We gratefully acknowledge Dave Crestani (The Blue Mountains Botanic Gardens, Mount Tomah) for identifying plant species during the vegetation survey and also The Blue Mountains Botanic Gardens team (Mount Tomah) for assistance planting Wollemi pine and help with ongoing management of the site. Jessica Rigg was supported by an Australian Postgraduate Award from the Australian Research Council.

Author information

Authors and Affiliations

  1. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, 2751, Australia

    J. L. Rigg, I. C. Anderson, B. K. Singh & J. R. Powell

  2. Australian Plant Bank, Royal Botanic Gardens and Domain Trust, Australian Botanic Garden, Mount Annan, NSW, 2587, Australia

    C. A. Offord

  3. School of Ecosystem and Forest Science, University of Melbourne, VIC, Richmond, 3121, Australia

    H. Zimmer

  4. Global Centre for Land-Based Innovation, Western Sydney University, Penrith, NSW, 2751, Australia

    B. K. Singh

Authors
  1. J. L. Rigg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. A. Offord
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Zimmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. C. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. K. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. R. Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. L. Rigg.

Additional information

Responsible Editor: Duncan D. Cameron.

Electronic supplementary material

Supplementary Table 1

(DOCX 13 kb)

Supplementary Table 2

(DOCX 16 kb)

Supplementary Figure 1

(DOCX 1011 kb)

Supplementary Figure 2

(DOCX 40 kb)

Supplementary Figure 3

Total water holding capacity (TWHC) and air-filled porosity (AFP) of soil at 768 the time Wollemi pine was planted. There was no significant difference between TWHC or AFP 769 according to gap type. (PDF 4 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rigg, J.L., Offord, C.A., Zimmer, H. et al. Conservation by translocation: establishment of Wollemi pine and associated microbial communities in novel environments. Plant Soil 411, 209–225 (2017). https://doi.org/10.1007/s11104-016-3010-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-3010-2

Keywords

Search

Navigation