Planting conditions improve translocation success of the endangered terrestrial orchid Diuris fragrantissima (Orchidaceae)
Zoë F. Smith A D , Elizabeth A. James B , Mark J. McDonnell C and Cassandra B. McLean C EA Australian Research Centre for Urban Ecology, Royal Botanic Gardens Melbourne, c/o School of Botany, The University of Melbourne, Vic. 3010, Australia.
B Royal Botanic Gardens Melbourne, Birdwood Avenue, South Yarra, Vic. 3141, Australia.
C School of Resource Management, Faculty of Land and Food Resources, Burnley College, The University of Melbourne, 500 Yarra Boulevard, Richmond, Vic. 3121, Australia.
D Corresponding author. Email: zsmith@unimelb.edu.au
E Deceased March 2009.
Australian Journal of Botany 57(3) 200-209 https://doi.org/10.1071/BT09072
Submitted: 14 April 2008 Accepted: 9 June 2009 Published: 29 June 2009
Abstract
By conducting reintroductions of the endangered terrestrial orchid Diuris fragrantissima D.L.Jones & M.A.Clem. we compared planting at the following three stages of the natural perennial growth cycle: as actively growing symbiotic plants in spring and autumn and as dormant tubers in summer. Plants reintroduced in spring and autumn were incorporated into randomised treatments involving soil aeration and addition of a mycorrhizal fungus. The addition of a mycorrhizal fungus and soil aeration together significantly increased survival and flowering of plants reintroduced in spring, whereas they had no significant effect on plants reintroduced in autumn. Addition of a fungus without soil aeration did not improve plant survival or flowering. Reintroducing actively growing plants was more successful than reintroducing dormant tubers, with 32.5% and 29.1% plants (reintroduced in spring and autumn, respectively) and 11.0% of tubers persisting after 4 years. Although survival of reintroduced plants declined at a rate of 16.9% per year for 4 years following reintroduction, survival of remnant plants remained relatively constant, ranging from 80.0 to 93.0%. Tuber size was positively correlated with survival and flowering of reintroduced plants for 2 years following reintroduction. A general trend was observed towards the increased likelihood of re-emergence and flowering of plants that flowered in previous seasons.
Acknowledgements
This paper is dedicated to the fond memory of Cassandra B. McLean; a dedicated mycorrhizal ecologist and inspiring and encouraging mentor. We thank the following people for their assistance with the reintroduction: Andrew Pritchard, Karen Lester and Gemma Phelan, Department of Sustainability and Environment; Fiona Smith and Katrina Lovett, Parks Victoria; Colin Knight, Melbourne Zoo; Dick Thomson, Russell Mawson, Peter Kiernan and Alex Smart, Australian Native Orchid Society; and all the volunteers who assisted with monitoring.
Anderson AB
(1991) Symbiotic and asymbiotic germination and growth of Spiranthes magnicamporum (Orchidaceae). Lindleyana 6, 183–186.
Anderson RC
(2008) Growth and arbuscular mycorrhizal fungal colonization of two prairie grasses grown in soil from restorations of three ages. Restoration Ecology 16, 650–656.
| Crossref | GoogleScholarGoogle Scholar |
Armstrong DP, Seddon PJ
(2008) Directions in reintroduction biology. Trends in Ecology & Evolution 23, 20–25.
| Crossref | GoogleScholarGoogle Scholar |
Batty AL,
Brundrett MC,
Dixon KW, Sivasithamparam K
(2006a) New methods to improve symbiotic propagation of temperate terrestrial orchid seedlings from axenic culture to soil. Australian Journal of Botany 54, 367–374.
| Crossref | GoogleScholarGoogle Scholar |
Batty AL,
Brundrett MC,
Dixon KW, Sivasithamparam K
(2006b) In situ symbiotic seed germination and propagation of terrestrial orchid seedlings for establishment at field sites. Australian Journal of Botany 54, 375–381.
| Crossref | GoogleScholarGoogle Scholar |
Batty AL,
Dixon KW,
Brundrett MC, Sivasithamparam K
(2001) Constraints to symbiotic germination of terrestrial orchid seed in a mediterranean bushland. New Phytologist 152, 511–520.
| Crossref | GoogleScholarGoogle Scholar |
Brundrett MC
(2007) Scientific approaches to Australian temperate terrestrial orchid conservation. Australian Journal of Botany 55, 293–307.
| Crossref | GoogleScholarGoogle Scholar |
Brundrett MC,
Scade A,
Batty AL,
Dixon KW, Sivasithamparam K
(2003) Development of in situ and ex situ seed baiting techniques to detect mycorrhizal fungi from terrestrial orchid habitats. Mycological Research 107, 1210–1220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cavender N, Knee M
(2006) Relationship of seed source and arbuscular mycorrhizal fungi inoculum type to growth and colonization of big bluestem (Andropogon gerardii). Plant and Soil 285, 57–65.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Clements MA, Ellyard RK
(1979) The symbiotic germination of Australian terrestrial orchids. American Orchid Society Bulletin 48, 810–816.
Colas B,
Kirchner F,
Riba M,
Olivieri I,
Mignot A,
Imbert E,
Beltrame C,
Carbonell D, Freville H
(2008) Restoration demography: a 10-year demographic comparison between introduced and natural populations of endemic Centaurea corymbosa (Asteraceae). Journal of Applied Ecology 45, 1468–1476.
| Crossref | GoogleScholarGoogle Scholar |
de Varennes A, Goss MJ
(2007) The tripartite symbiosis between legumes, rhizobia and indigenous mycorrhizal fungi is more efficient in undisturbed soil. Soil Biology & Biochemistry 39, 2603–2607.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Debeljak N,
Regvar M,
Dixon KW, Sivasithamparam K
(2002) Induction of tuberisation in vitro with jasmonic acid and sucrose in an Australian terrestrial orchid, Pterostylis sanguinea. Plant Growth Regulation 36, 253–260.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Decruse SW,
Gangaprasad A,
Seeni S, Menon VS
(2003) Micropropagation and ecorestoration of Vanda spathulata, an exquisite orchid. Plant Cell, Tissue and Organ Culture 72, 199–202.
| Crossref | GoogleScholarGoogle Scholar |
Diaz A,
Green I,
Benvenuto M, Tibbett M
(2006) Are Ericoid mycorrhizas a factor in the success of Calluna vulgaris heathland restoration? Restoration Ecology 14, 187–195.
| Crossref | GoogleScholarGoogle Scholar |
Diez JM
(2007) Hierarchical patterns of symbiotic orchid germination linked to adult proximity and environmental gradients. Journal of Ecology 95, 159–170.
| Crossref | GoogleScholarGoogle Scholar |
Dutra D,
Johnson TR,
Kauth PJ,
Stewart SL,
Kane ME, Richardson L
(2008) Asymbiotic seed germination, in vitro seedling development, and greenhouse acclimatization of the threatened terrestrial orchid Bletia purpurea. Plant Cell, Tissue and Organ Culture 94, 11–21.
| Crossref | GoogleScholarGoogle Scholar |
Dutra D,
Kane ME, Richardson L
(2009) Asymbiotic seed germination and in vitro seedling development of Cyrtopodium punctatum: a propagation protocol for an endangered Florida native orchid. Plant Cell, Tissue and Organ Culture 96, 235–243.
Entry JA,
Rygiewicz PT,
Watrud LS, Donnelly PK
(2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Advances in Environmental Research 7, 123–138.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Hobbs RJ, Huenneke LF
(1992) Disturbance, diversity and invasion: implications for conservation. Conservation Biology 6, 324–337.
| Crossref | GoogleScholarGoogle Scholar |
Hutchings MJ
(1987) The population biology of the early spider orchid Ophrys sphegodes Mill. 1. A demographic study from 1975–1984. Journal of Ecology 75, 711–727.
| Crossref | GoogleScholarGoogle Scholar |
Huynh T,
McLean CB,
Coates F, Lawrie A
(2004) Effect of developmental stage and peloton morphology on success in isolation of mycorrhizal fungi in Caladenia formosa (Orchidaceae). Australian Journal of Botany 52, 231–241.
| Crossref | GoogleScholarGoogle Scholar |
Jasper DA
(2007) Beneficial soil microorganisms of the jarrah forest and their recovery in bauxite mine restoration in south western Australia. Restoration Ecology 15, S74–S84.
Jersáková J, Malinová T
(2007) Spatial aspects of seed dispersal and seedling recruitment in orchids. New Phytologist 176, 237–241.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Johnson NC
(1998) Responses of Salsola kali and Panicum virgatum to mycorrhizal fungi, phosphorus and soil organic matter: implications for reclamation. Journal of Applied Ecology 35, 86–94.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Kauth PJ,
Vendrame WA, Kane ME
(2006) In vitro seed culture and seedling development of Calopogon tuberosus. Plant Cell, Tissue and Organ Culture 85, 91–102.
| Crossref | GoogleScholarGoogle Scholar |
Kery M, Gregg KB
(2004) Demographic analysis of dormancy and survival in the terrestrial orchid Cypripedium reginae. Journal of Ecology 92, 686–695.
| Crossref | GoogleScholarGoogle Scholar |
Lunt PH, Hedger JN
(2003) Effects of organic enrichment of mine spoil on growth and nutrient uptake in oak seedlings inoculated with selected mycorrhizal fungi. Restoration Ecology 11, 125–130.
| Crossref | GoogleScholarGoogle Scholar |
MacDougall AS, Turkington R
(2007) Does the type of disturbance matter when restoring disturbance-dependent grasslands? Restoration Ecology 15, 263–272.
| Crossref | GoogleScholarGoogle Scholar |
Maestre FT,
Bautista S,
Cortina J,
Diaz G,
Honrubia M, Vallejo R
(2002) Microsite and mycorrhizal inoculum effects on the establishment of Quercus coccifera in a semi-arid degraded steppe. Ecological Engineering 19, 289–295.
| Crossref | GoogleScholarGoogle Scholar |
Martin KP
(2003) Clonal propagation, encapsulation and reintroduction of Ipsea malabarica (Reichb. f.) J.D.Hook, an endangered orchid. In Vitro Cellular & Developmental Biology. Plant 39, 322–326.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCormick MK,
Whigham DF,
Sloan D,
O’Malley K, Hodkinson B
(2006) Orchid–fungus fidelity: a marriage meant to last? Ecology 87, 903–911.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McKendrick SL
(1995) The effects of herbivory and vegetation on laboratory-raised Dactylorhiza praetermissa (Orchidaceae) planted into grassland in southern England. Biological Conservation 73, 215–220.
| Crossref | GoogleScholarGoogle Scholar |
Menges E
(2008) Restoration demography and genetics of plants: when is a translocation successful? Australian Journal of Botany 56, 187–196.
| Crossref | GoogleScholarGoogle Scholar |
Morgan JW
(1997) The effect of grassland gap size on establishment, growth and flowering of the endangered Rutidosis leptorrhynchoides (Asteraceae). Journal of Applied Ecology 34, 566–576.
| Crossref | GoogleScholarGoogle Scholar |
Nadian H,
Smith SE,
Alston AM,
Murray RS, Siebert BD
(1998) Effects of soil compaction on phosphorus uptake and growth of Trifolium subterraneum colonized by four species of vesicular-arbuscular mycorrhizal fungi. New Phytologist 140, 155–165.
| Crossref | GoogleScholarGoogle Scholar |
Ortega-Larrocea MP,
Seibe C,
Estrada A, Webster R
(2007) Mycorrhizal inoculum potential of arbuscular mycorrhizal fungi in soils irrigated with wastewater for various lengths of time, as affected by heavy metals and available P. Applied Soil Ecology 37, 129–138.
| Crossref | GoogleScholarGoogle Scholar |
Pavao-Zuckerman MA
(2008) The nature of urban soils and their role in ecological restoration in cities. Restoration Ecology 16, 642–649.
| Crossref | GoogleScholarGoogle Scholar |
Primack R, Stacy E
(1998) Cost of reproduction in the pink lady’s slipper orchid (Cypripedium acaule, Orchidaceae): an eleven-year experimental study of three populations. American Journal of Botany 85, 1672–1679.
| Crossref | GoogleScholarGoogle Scholar |
Ramsay MM, Stewart J
(1998) Re-establishment of the lady’s slipper orchid (Cypripedium calceolus L.) in Britain. Botanical Journal of the Linnean Society 126, 173–181.
Rasmussen HN, Whigham DF
(1993) Seed ecology of dust seeds in situ: a new study technique and its application in terrestrial orchids. American Journal of Botany 80, 1374–1378.
| Crossref | GoogleScholarGoogle Scholar |
Ryszka P, Turnau K
(2007) Arbuscular mycorrhiza of introduced and native grasses colonizing zinc wastes: implications for restoration practices. Plant and Soil 298, 219–229.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Scade A,
Brundrett M,
Batty AL,
Dixon KW, Sivasithamparam K
(2006) Survival of transplanted terrestrial orchid seedlings in urban bushland habitats with a high or low weed cover. Australian Journal of Botany 54, 383–389.
| Crossref | GoogleScholarGoogle Scholar |
Sinclair A, Catling PM
(2003) Restoration of Hydrastis canadensis by transplanting with disturbance simulation: results of one growing season. Restoration Ecology 11, 217–222.
| Crossref | GoogleScholarGoogle Scholar |
Smith ZF,
James EA, McLean CB
(2005) Investigation of the Diuris ‘punctata’ group in south-eastern Australia based on nuclear and chloroplast sequencing. Selbyana 26, 217–228.
Smith ZF,
James EA, McLean CB
(2007) Investigation of the phylogenetic relationships between Diuris fragrantissima and its closest relatives using AFLPs. Environmentalist 27, 217–226.
| Crossref | GoogleScholarGoogle Scholar |
Standish RJ,
Stokes BA,
Tibbett M, Hobbs RJ
(2007) Seedling response to phosphate addition and inoculation with arbuscular mycorrhizas and the implications for old-field restoration in Western Australia. Environmental and Experimental Botany 61, 58–65.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Stenberg ML, Kane ME
(1998) In vitro seed germination and greenhouse cultivation of Encyclia boothiana var. erythronioides, an endangered Florida orchid. Lindleyana 13, 101–112.
Stewart SL, Kane ME
(2006) Asymbiotic seed germination and in vitro seedling development of Habernaria macroceratitis (Orchidaceae), a rare Florida terrestrial orchid. Plant Cell, Tissue and Organ Culture 86, 147–158.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Stewart SL, Zettler LW
(2002) Symbiotic germination of three semi-aquatic rein orchids (Habernaria repens, H. quinquesesta, H. macroceratitis) from Florida. Aquatic Botany 72, 25–35.
| Crossref | GoogleScholarGoogle Scholar |
Stewart SL,
Zettler LW,
Minso J, Brown PM
(2003) Symbiotic germination and reintroduction of Spiranthes brevilabris Lindley, an endangered orchid native to Florida. Selbyana 24, 64–70.
Takahashi K,
Ishikawa H,
Ogino T,
Hatana T, Ogiwara I
(2008) Time of seed germination, infection of orchid mycorrhizal fungi, and reintroduction of protocorms inoculated with orchid mycorrhizal fungi and covered with gel to a habitat in Habernaria radiata (Thunb.) K.Spreng. Horticultural Research (Japan) 7, 27–31.
| Crossref | GoogleScholarGoogle Scholar |
Wendelberger KS,
Fellows MQN, Maschinski J
(2008) Rescue and restoration: experimental translocation of Amorpha herbacea Walter var. crenulata (Rybd.) Isley into a novel urban habitat. Restoration Ecology 16, 542–552.
| Crossref | GoogleScholarGoogle Scholar |
White JA,
Tallaksen J, Charvat I
(2008) The effects of arbuscular mycorrhizal fungal inoculation at a roadside prairie restoration site. Mycologia 100, 6–11.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wright M,
Cross R,
Dixon K,
Huynh T,
Lawrie A,
Nesbitt L,
Pritchard A,
Swarts N, Thomson R
(2009) Caladenia propagation and reintroduction. Australian Journal of Botany in press. 57,
Xu D,
Dell B,
Malajczuk N, Gong M
(2001) Effects of P fertilisation and ectomycorrhizal fungal inoculation on early growth of eucalypt plantations in southern China. Plant and Soil 233, 47–57.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Zettler LW,
Poulter SB,
McDonald KI, Stewart SL
(2007) Conservation-driven propagation of an epiphytic orchid (Epidendrum nocturnum) with a mycorrhizal fungus. HortScience 42, 135–139.