Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Scientific approaches to Australian temperate terrestrial orchid conservation

Mark C. Brundrett
+ Author Affiliations
- Author Affiliations

Terrestrial Ecosystems Branch, Policy and Coordination Division, EPA Service Unit, Department of Environment, PO Box K822, Perth, WA 6000, Australia and Faculty of Natural and Agricultural Sciences, School of Plant Biology, The University of Western Australia, Crawley, WA 6009, Australia. Email: brundrm@cyllene.uwa.edu.au

Australian Journal of Botany 55(3) 293-307 https://doi.org/10.1071/BT06131
Submitted: 21 June 2006  Accepted: 23 October 2006   Published: 18 May 2007

Abstract

This review summarises scientific knowledge concerning the mycorrhizal associations, pollination, demographics, genetics and evolution of Australian terrestrial orchids relevant to conservation. The orchid family is highly diverse in Western Australia (WA), with over 400 recognised taxa of which 76 are Declared Rare or Priority Flora. Major threats to rare orchids in WA include habitat loss, salinity, feral animals and drought. These threats require science-based recovery actions resulting from collaborations between universities, government agencies and community groups.

Fungal identification by DNA-based methods in combination with compatibility testing by germination assays has revealed a complex picture of orchid–fungus diversity and specificity. The majority of rare and common WA orchids studied have highly specific mycorrhizal associations with fungi in the Rhizoctonia alliance, but some associate with a wider diversity of fungi. These fungi may be a key factor influencing the distribution of orchids and their presence can be tested by orchid seed bait bioassays. These bioassays show that mycorrhizal fungi are concentrated in coarse organic matter that may be depleted in some habitats (e.g. by frequent fire). Mycorrhizal fungi also allow efficient propagation of terrestrial orchids for reintroduction into natural habitats and for bioassays to test habitat quality.

Four categories of WA orchids are defined by the following pollination strategies: (i) nectar-producing flowers with diverse pollinators, (ii) non-rewarding flowers that mimic other plants, (iii) winter-flowering orchids that attract fungus-feeding insects and (iv) sexually deceptive orchids with relatively specific pollinators. An exceptionally high proportion of WA orchids have specific insect pollinators. Bioassays testing orchid-pollinator specificity can define habitats and separate closely related species. Other research has revealed the chemical basis for insect attraction to orchids and the ecological consequences of deceptive pollination. Genetic studies have revealed that the structure of orchid populations is influenced by pollination, seed dispersal, reproductive isolation and hybridisation. Long-term demographic studies determine the viability of orchid populations, estimate rates of transition between seedling, flowering, non-flowering and dormant states and reveal factors, such as grazing and competition, that result in declining populations.

It is difficult to define potential new habitats for rare orchids because of their specific relationships with fungi and insects. An understanding of all three dimensions of orchid habitat requirements can be provided by bioassays with seed baits for fungi, flowers for insects and transplanted seedlings for orchid demography. The majority of both rare and common WA orchids have highly specific associations with pollinating insects and mycorrhizal fungi, suggesting that evolution has favoured increasing specificity in these relationships in the ancient landscapes of WA.


Acknowledgements

Andrew Brown and Steve Hopper provided valuable comments and information. I also particularly thank the following people: Andrew Batty and Professor Sivasithamparam at the University of Western Australia. I gratefully acknowledge the many colleagues, students and volunteers who have collaborated with me in orchid research: Kingsley Dixon, Eric Bunn, Keran Keys, Bob Dixon and Siegy Krauss at the Botanic Gardens and Parks Authority; postgraduate students: Nura Abdul Karim, Jeremy Bougoure, Margaret Collins, Sofi Mursidawati, Belinda Newman; honours students: Yumi Bonnardeaux, Ailsa Scade, Erin Wright, Danika Collins; and Andrew Brown, Jillian Stack, Beth Laudon and others at the Department of Conservation and Land Management. Volunteers of the West Australian Native Orchid Study and Conservation Group, Friends of Kings Park and Kings Park Master Gardeners. Funding was provided by ARC, The Botanic Gardens and Parks Authority, ALCOA World Alumina Inc., The National Heritage Trust and Lotterywest.


References


Adams PB, Lawson SD (1993) Pollination of Australian orchids: a critical assessment of the literature 1882–1992. Australian Journal of Botany 41, 553–575.
Crossref | GoogleScholarGoogle Scholar | open url image1

Arditti J, Ghani AKA (2000) Numerical and physical properties of orchid seeds and their biological implications. New Phytologist 145, 367–421.
Crossref | GoogleScholarGoogle Scholar | open url image1

Batty AL, Dixon KW, Brundrett MC, Sivasithamparam K (2001a) Constraints to symbiotic germination of terrestrial orchid seeds in mediterranean woodland. New Phytologist 152, 511–520.
Crossref | GoogleScholarGoogle Scholar | open url image1

Batty AL, Dixon KW, Brundrett MC, Sivasithamparam K (2001b) The long-term storage of mycorrhizal fungi and seed as a tool for the conservation of endangered terrestrial orchids. Australian Journal of Botany 49, 619–628.
Crossref | GoogleScholarGoogle Scholar | open url image1

Batty AL , Dixon KW , Brundrett MC , Sivasithamparam K (2002) Orchid conservation and mycorrhizal associations. In ‘Microorganisms in plant conservation and biodiversity’. (Eds K Sivasithamparam, KW Dixon, RL Barrett) pp. 195–226. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Batty AL, Brundrett MC, Dixon KW, Sivasithamparam K (2006a) 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 | open url image1

Batty AL, Brundrett MC, Dixon KW, Sivasithamparam K (2006b) New methods to improve symbiotic propagation of temperate terrestrial orchids from axenic culture to soil. Australian Journal of Botany 54, 367–374.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bayerman P , Otero T (2006) Microbial endophytes of orchids. In ‘Microbial root endophytes’. (Eds B Schulz, C Boyle, T Sieber) pp. 153–177. (Springer-Verlag: Berlin)

Beardsell DV, Clements MA, Hutchinson JF, Williams EG (1986) Pollination of Diuris maculata R.Br. (Orchidaceae) by floral mimicry of the native peas Daviesia spp. and Pultanaea scabra R.Br. Australian Journal of Botany 34, 165–173.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bell DT (2001) Ecological response syndromes in the flora of southwestern Western Australia: fire resprouters versus reseeders. Botanical Review 67, 417–440. open url image1

Benzing DH, Atwood JT (1984) Orchidaceae: ancestral habitats and current status in forest canopies. Systematic Botany 9, 155–165.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bernhardt P (1990) ‘Wily violets and underground orchids: revelations of a botanist.’ (Allen and Unwin: Sydney)

Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ (2004) Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proceedings of the Royal Society of London. Series B. Biological Sciences 271, 1799–1806.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bonnardeaux Y, Brundrett M, Batty A, Dixon K, Koch J, Sivasithamparam K (2007) Diversity of mycorrhizal fungi of Western Australian terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions. Mycological Research 111, 51–61.
Crossref | PubMed |
open url image1

Bougoure JJ, Bougoure DS, Cairney JWG, Dearnaley JDW (2005) ITS–RFLP and sequence of endophytes from Acianthus, Caladenia and Pterostyis (Orchidaceae) in southeastern Queensland. Mycological Research 109, 452–460.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bower CC (1996) Demonstration of pollinator-mediated reproductive isolation in sexually deceptive species of Chiloglottis (Orchidaceae). Australian Journal of Botany 44, 15–33.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bowles M, Zettler L, Bell T, Kelsey P (2005) Relationship between soil characteristics, distribution and restoration potential of the federal threatened eastern prairie fringed orchid Platanthera leucophaea (Nutt.) Lindl. American Midland Naturalist 154, 273–286.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brown A (1991) Western Australian native orchids: the masters of deceit. In ‘Proceedings of the 12th Australian orchid conference’. pp. 24–29. (Orchid Society of Western Australia: Perth)

Brown EM , Burbidge AH , Dell J , Edinger D , Hopper SD , Wills RT (1997) ‘Pollination in Western Australia: a database of animals visiting flowers. Handbook no. 15.’ (Western Australian Naturalists’ Club: Perth)

Brown A , Thomson-Dans C , Marchant N (1998) ‘Western Australia’s threatened flora.’ (Department of Conservation and Land Management: Perth)

Brzosko E (2002) Dynamics of island populations of Cypripedium calceolus in the Biebrza river valley (north-east Poland). 2002. Botanical Journal of the Linnean Society 139, 67–77.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brundrett MC (1991) Mycorrhizas in natural ecosystems. Advances in Ecological Research 21, 171–313. open url image1

Brundrett M (2002) Coevolution of roots and mycorrhizas of land plants. New Phytologist 154, 275–304.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biological Reviews 79, 473–495.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brundrett MC (2006) Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In ‘Microbial root endophytes’. (Eds B Schulz, C Boyle, T Sieber) pp. 281–297. (Springer-Verlag: Berlin)

Brundrett MC, Abbott LK (1991) Roots of jarrah forest plants. I. Mycorrhizal associations of shrubs and herbaceous plants. Australian Journal of Botany 39, 445–457.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 | open url image1

Burgman MA , Lindenmayer DB (1998) ‘Conservation biology for the Australian environment.’ (Surrey Beatty: Sydney)

Calvo RN (1993) Evolutionary demography of orchids: intensity and frequency of pollination and cost of fruiting. Ecology 74, 1033–1042.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycorrhiza in orchids: evidence from plant–fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytologist 171, 405–416.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chase MW , Cameron KM , Barrett RL , Freudenstein JV (2003) DNA data and Orchidaceae systematics: a new phylogenetic classification. In ‘Orchid conservation’. (Eds KW Dixon, SP Kell, RL Barrett, PJ Cribb) pp. 69–89. (Natural History Publications: Kota Kinabalu, Sabah, Malaysia)

Chung MY, Nason JD, Chung MG (2004) Spatial genetic structure in populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae). American Journal of Botany 91, 52–57. open url image1

Clark S, deLacey C, Chamberlain S (2004) Using environmental variables and multivariate analysis to delineate preferred habitat for Cryptostylis hunteriana, the leafless tongue orchid, in the Shoalhaven Local Government Area, NSW. Cunninghamia 8, 467–476. open url image1

Coates DJ, Atkins KA (2001) Priority setting and the conservation of Western Australia’s diverse and highly endemic flora. Biological Conservation 97, 251–263.
Crossref | GoogleScholarGoogle Scholar | open url image1

Coates F, Lunt ID, Tremblay RL (2006) Effects of disturbance on population dynamics of the threatened orchid Prasophyllum correctum D.L.Jones and implications for grassland management in south-eastern Australia. Biological Conservation 129, 59–69.
Crossref | GoogleScholarGoogle Scholar | open url image1

Collins M, Koch J, Brundrett M, Sivasithamparam K (2005) Recovery of terrestrial orchids in the post-mining landscape. Selbyana 25, 255–264. open url image1

Commonwealth of Australia (2002) ‘Australian terrestrial biodiversity assessment 2002.’ (National Land and Water Resources Audit: Canberra)

Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends in Ecology & Evolution 20, 487–494.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cozzolino S, Noce ME, Musacchio A, Widmer A (2003) Variation at a chloroplast minisatellite locus reveals the signature of habitat fragmentation and genetic bottlenecks in the rare orchid Anacamptis palustris (Orchidaceae). American Journal of Botany 90, 1681–1687. open url image1

Cozzolino S, Scheistl FP, Müller A, De Castro O, Nardella AM, Widmer A (2005) Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: absence of premating barriers? Proceedings of the Royal Society of London. Series B. Biological Sciences 272, 1271–1278.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cozzolino S, Nardella AM, Impagliazzo S, Widmer A, Lexer C (2006) Hybridization and conservation of Mediterranean orchids: should we protect the orchid hybrids or the orchid hybrid zones? Biological Conservation 129, 14–23.
Crossref | GoogleScholarGoogle Scholar | open url image1

Currah RS , Zelmer CD , Hambleton S , Richardson KA (1996) Fungi from orchid mycorrhizas. In ‘Orchid biology: reviews and perspectives. VII’. (Eds J Arditti, A Pridgeon) pp. 117–170. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Dafni A (1984) Mimicry and deception in pollination. Annual Review of Ecology and Systematics 15, 259–278.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dafni A, Calder DM (1987) Pollination by deceit and floral mimesis in Thelymitra atennifera (Orchidaceae). Plant Systematics and Evolution 158, 11–22.
Crossref | GoogleScholarGoogle Scholar | open url image1

Darwin C (1904) ‘The various contrivances by which orchids are fertilized by insects.’ 2nd edn. (John Murray: London)

Dixon K (1991) Seeder/clonal concepts in Western Australian orchids. In ‘Population ecology of terrestrial orchid’. (Eds TCE Wells, JH Willems) pp. 111–123. (SPB Academic Publishing: The Hague, The Netherlands)

Edwards W, Westoby M (2000) Families with highest proportions of rare species are not consistent between floras. Journal of Biogeography 27, 733–740.
Crossref | GoogleScholarGoogle Scholar | open url image1

Elliott CP, Ladd PG (2002) Pollen limitation of fruit set in Western Australian terrestrial orchids. Journal of the Royal Society of Western Australia 85, 165–168. open url image1

Erickson R (1965) ‘Orchids of the west.’ (Paterson Brokensha: Perth)

Esitken A, Ercisli S, Eken C (2005) Effects of mycorrhiza isolates on symbiotic germination of terrestrial orchids (Orchis palustris Jacq. and Serapias vomeracea subsp. vomeracea (Burm.f.) Briq.) in Turkey.  Symbiosis 38, 59–68. open url image1

Feuerherdt L, Petit S, Jusaitis M (2005) Distribution of mycorrhizal fungus associated with the endangered pink-lipped spider orchid (Arachnorchis (syn. Caladenia) behrii) at Warren Conservation Park in South Australia. New Zealand Journal of Botany 43, 367–371. open url image1

George AS (1980) Rhizanthella gardneri R.S.Rogers – the underground orchid of Western Australia. American Orchid Society Bulletin 49, 631–644. open url image1

Gonzales D, Carling DE, Kuninaga S, Vilgalys R, Cubeta MA (2001) Ribosomal DNA systematics of Ceratobasidium and Thanatephorus with Rhizoctonia anamorphs. Mycologia 93, 1138–1150.
Crossref |
open url image1

Grant CD, Koch J (2003) Orchid species succession in rehabilitated bauxite mines in Western Australia. Australian Journal of Botany 51, 453–457.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hoffman N , Brown A (1998) ‘Orchids of South-west Australia.’ 2nd edn. (University of Western Australia Press: Perth)

Hollick P (2004) Mycorrhizal specificity in endemic Western Australian terrestrial orchids (tribe Diurideae): implications for conservation. PhD Thesis, Murdoch University, Perth.

Hopper SD, Brown AP (2004) Robert Brown’s Caladenia revisited, including a revision of its sister genera Cyanicula, Ericksonella and Pheladenia (Caladeniinae: Orchidaceae). Australian Systematic Botany 17, 171–240.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hopper SD, Gioia P (2004) The Southwest Australian Floristic Region: evolution and conservation of a global hotspot of biodiversity. Annual Review of Evolution and Systematics 35, 623–650.
Crossref | GoogleScholarGoogle Scholar | open url image1

Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route or route to extinction? Oikos 108, 427–432.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hutchings MJ (1987) The population biology of the early spider orchid, Ophrys sphegodes Mill. I. A demographic study from 1975 to 1984. Journal of Ecology 75, 711–727.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huynh TT, McLean CB, Coates F, Lawrie AC (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 | open url image1

Jacquemyn H, Brys R, Hermy M, Willems JH (2005a) Does nectar reward affect rarity and extinction probabilities of orchid species? An assessment using historical records from Belgium and the Netherlands. Biological Conservation 121, 257–263.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jacquemyn H, Micheneau C, Roberts DL, Pailler T (2005b) Elevational gradients of species diversity, breeding system and floral traits of orchid species on Reunion Island. Journal of Biogeography 32, 1751–1761.
Crossref | GoogleScholarGoogle Scholar | open url image1

Johnson SD, Neal PR, Harder LD (2005) Pollen fates and the limits on male reproductive success in an orchid population. Biological Journal of the Linnean Society 86, 175–190.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jones DL (1988) ‘Native orchids of Australia.’ (Reed Books Pty Ltd: Sydney)

Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse M-A (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytologist 166, 639–653.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kelly CL, Pickering CM, Buckley RC (2003) Impacts of tourism on threatened plant taxa and communities in Australia. Ecological Management & Restoration 4, 37–44.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kéry 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 | open url image1

Kéry M, Gregg KB, Schaub M (2005) Demographic estimation methods for plants with unobservable life-states. Oikos 108, 307–320.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kristiansen KA, Freudenstein JV, Rasmussen FN, Rasmussen HN (2004) Molecular identification of mycorrhizal fungi in Newiedia veratrifolia (Orchidaceae). Molecular Phylogenetics and Evolution 33, 251–258.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kull T, Hutchings MJ (2006) A comparative analysis of decline in the distribution ranges of orchid species in Estonia and the United Kingdom. Biological Conservation 129, 31–39.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leake JR (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytologist 127, 171–216.
Crossref | GoogleScholarGoogle Scholar | open url image1

Light MHS, MacConaill M (2005) Long-term studies: a case for orchid species survival. Selybyana 26, 174–188. open url image1

Linder HP (1995) Setting conservation priorities: the importance of endemism and phylogeny in the southern African orchid genus Herschelia. Conservation Biology 9, 585–595.
Crossref | GoogleScholarGoogle Scholar | open url image1

Machon N, Bardin P, Mazer SJ, Moret J, Godelle B, Austerlitz F (2003) Relationship between genetic structure and seed and pollen dispersal in the endangered orchid Spiranthes spiralis. New Phytologist 157, 677–687.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mant J, Peakall R, Weston PH (2005a) Specific pollinator attraction and the diversification of sexually deceptive Chiloglottis (Orchidaceae). Plant Systematics and Evolution 253, 185–200.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mant J, Bower CC, Weston PH, Peakall R (2005b) Phylogeography of pollinator-specific sexually deceptive Chiloglottis taxa (Orchidaceae): evidence for sympatric divergence? Molecular Ecology 14, 3067–3076.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Masuhara G, Katsuya K (1994) In situ and in vitro specificity between Rhizoctonia spp. and Spiranthes sinensis (Persoon.) Ames. var. amoena (M.Beiberstein) Hara (Orchidaceae). New Phytologist 127, 711–718.
Crossref | GoogleScholarGoogle Scholar | open url image1

McCormick MK, Whigham DF, O’Neill J (2004) Mycorrhizal diversity in photosynthetic terrestrial orchids. New Phytologist 163, 425–438.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 | open url image1

Milligan MJ, Williams PG (1988) The mycorrhizal relationship of multinucleate rhizoctonias from non-orchids with Microtis (Orchidaceae). New Phytologist 108, 205–210.
Crossref | GoogleScholarGoogle Scholar | open url image1

Molvray M , Kores PJ , Chase MW (2000) Polyphyly of mycoheterotrophous orchids and functional influences on floral and molecular characters. In ‘Monocots: systematics and evolution’. (Eds KL Wilson, DA Mossison) pp. 441–448. (CSIRO Publishing: Melbourne)

Murren CJ (2002) Effects of habitat fragmentation on pollination: pollinia viability and reproductive success. Journal of Ecology 90, 100–107.
Crossref | GoogleScholarGoogle Scholar | open url image1

Murren CJ, Ellison AM (1998) Seed dispersal characteristics of Brassavola nodosa (Orchidaceae). American Journal of Botany 85, 675–680.
Crossref | GoogleScholarGoogle Scholar | open url image1

Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Myklestad A, Saetersdal M (2005) Effects of fertilization and afforestation on community structure of traditionally managed hay meadows in western Norway. Nordic Journal of Botany 23, 593–606. open url image1

Nicolè F, Brzosko E, Till-Bottraud I (2005) Population viability analysis of Cypripedium calceolus in a protected area: longevity, stability and persistence. Journal of Ecology 93, 716–726.
Crossref | GoogleScholarGoogle Scholar | open url image1

Neiland MRM, Wilcox CC (1998) Fruit set, nectar reward, and rarity in the Orchidaceae. American Journal of Botany 85, 1657–1671.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nilsson LA (1992) Orchid pollination biology. Trends in Ecology & Evolution 7, 255–259.
Crossref | GoogleScholarGoogle Scholar | open url image1

Otero JT, Flanagan NS (2006) Orchid diversity – beyond deception. Trends in Ecology & Evolution 21, 64–65.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pacini E, Hesse M (2002) Types of pollen dispersal units in orchids, and their consequences for germination and fertilization. Annals of Botany 89, 653–664.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pate JS , Hopper SD (1994) Rare and common plants in ecosystems, with special reference to the south-west Australian flora. In ‘Biodiversity and ecosystem function’. (Eds E-D Schulze, HA Mooney) pp. 293–325. (Springer-Verlag: Berlin)

Peakall R (1990) Responses of male Zaspilothynnus trilobatus Turner wasps to females and the sexually deceptive orchid it pollinates. Functional Ecology 4, 159–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Peakall R, Beattie AJ (1991) The genetic consequences of worker ant pollination in a self-compatible clonal orchid. Evolution 45, 1837–1848.
Crossref | GoogleScholarGoogle Scholar | open url image1

Peakall R, Beattie AJ (1996) Ecological and genetic consequences of pollination by sexual deception in the orchid Caladenia tentaculata. Evolution 50, 2207–2220.
Crossref | GoogleScholarGoogle Scholar | open url image1

Perkins AJ, McGee PA (1995) Distribution of the orchid mycorrhizal fungus, Rhizoctonia solani, in relation to its host, Pterostylis acuminata, in the field. Australian Journal of Botany 43, 565–575.
Crossref | GoogleScholarGoogle Scholar | open url image1

Perkins AJ, Masuhara G, McGee PA (1995) Specificity of the associations between Microtis parvifolia (Orchidaceae) and its mycorrhizal fungi. Australian Journal of Botany 43, 85–91.
Crossref | GoogleScholarGoogle Scholar | open url image1

Peterson RL, Uetake Y, Zelmer C (1998) Fungal symbioses with orchid protocorms. Symbiosis 25, 29–55. open url image1

Petit S, Dickson CR (2005) Grass-tree (Xanthorrhoea semiplana, Liliaceae) facilitation of the endangered pink-lipped spider orchid (Caladenia syn. Arachnorchis behrii, Orchidaceae) varies in South Australia. Australian Journal of Botany 53, 455–464.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pfeifer M, Wiegand K, Heinrich W, Jetchke G (2006) Long-term demographic fluctuations in an orchid species driven by weather implications for conservation planning. Journal of Applied Ecology 43, 313–324.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pope EJ, Carter DA (2001) Phylogenetic placement and host specificity of mycorrhizal isolates belonging to AG-6 and AG-12 in the Rhizoctonia solani species complex. Mycologia 93, 712–719.
Crossref |
open url image1

Primack R, Stacy E (1998) Cost of reproduction in the pink lady’s slipper orchid (Cypripedium acule, Orchidaceae): an eleven-year experimental study of three populations. American Journal of Botany 85, 1672–1679.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ramsay MM , Dixon KW (2003) Propagation science, recovery and translocation of terrestrial orchids. In ‘Orchid conservation’. (Eds KW Dixon, SP Kell, RL Barrett, PJ Cribb) pp. 259–288. (Natural History Publications: Kota Kinabalu, Sabah, Malaysia)

Ramsay RR, Sivasithamparam K, Dixon KW (1987) Anastomosis groups among Rhizoctonia-like endophytic fungi in southwestern Australian Pterostylis species (Orchidaceae). Lindleyana 2, 161–166. open url image1

Rasmussen HN (1995) ‘Terrestrial orchids, from seed to mycotrophic plant.’ (Cambridge University Press: Cambridge)

Rasmussen HN (2002) Recent developments in the study of orchid mycorrhiza. Plant and Soil 244, 149–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rasmussen HN, Whigham D (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 | open url image1

Reinhammar L-G, Olsson EGA, Sørmeland E (2002) Conservation biology of an endangered grassland plant species, Pseudorchis albida, with some references to the closely related alpine P. straminea (Orchidaceae). Botanical Journal of the Linnean Society 139, 47–66.
Crossref | GoogleScholarGoogle Scholar | open url image1

Risdall-Smith JJ (1970) The behaviour of Hemithynnus hyalinatus (Hymenoptera: Tiphiidae), with notes on some other Thynninae. Journal of the Australian Entomological Society 9, 196–208.
Crossref |
open url image1

Roberts P (1999) ‘Rhizoctonia-forming fungi.’ (Whitstable Litho Printers Ltd: Kent, UK)

Scade A, Brundrett MC, Batty AL, Dixon KW, Sivasithamparam K (2006) Survival of transplanted terrestrial orchid seedlings in urban bushland habitats with high or low weed cover. Australian Journal of Botany 54, 383–389.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Die Naturwissenschaften 92, 255–264.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schiestl FP, Peakall R, Mant J (2004) Chemical communication in the sexually deceptive orchid genus Cryptostylis. Botanical Journal of the Linnean Society 144, 199–205.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schwartz MW, Simberloff D (2001) Taxon size predicts rates of rarity in vascular plants. Ecology Letters 4, 464–469.
Crossref | GoogleScholarGoogle Scholar | open url image1

Selosse M-A, Faccio A, Scappaticci G, Bonfante P (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbial Ecology 47, 416–426.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sharma IK, Jones DL, French CJ (2003) Unusually high genetic variability revealed through allozymic polymorphism of an endemic and endangered Australian orchid, Pterostylis aff. picta (Orchidaceae). Biochemical Systematics and Ecology 31, 513–526.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shefferson RP, Kull T, Tali K (2005a) Adult whole-plant dormancy induced by stress in long-lived orchids. Ecology 86, 3099–3104. open url image1

Shefferson RP, Weiss M, Kull T, Taylor DL (2005b) High specificity generally characterizes mycorrhizal association in rare lady’s slipper orchids, genus Cypripedium. Molecular Ecology 14, 613–626.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sivasithamparam K (1993) Ecology of root infecting pathogenic fungi in mediterranean environments. Advances in Plant Pathology 10, 245–279. open url image1

Soliva M, Widmer A (2003) Gene flow across species boundaries in sympatric, sexually deceptive Ophrys (Orchidaceae) species. Evolution 57, 2252–2261.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stewart SL, Zettler LW (2002) Symbiotic germination of three semi-aquatic rein orchids (Habenaria repens, H. quinquiseta, H. macroceratitius) from Florida. Aquatic Botany 72, 25–35.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stoutamire WP (1983) Wasp-pollinated species of Caladenia (Orchidaceae) in south-western Australia. Australian Journal of Botany 31, 383–394.
Crossref | GoogleScholarGoogle Scholar | open url image1

Taylor DL , Bruns TD , Leake JR , Read DJ (2002) Mycorrhizal specificity and function in myco-heterotrophic plants. In ‘Mycorrhizal ecology. Ecological studies vol. 157’. (Eds MGA van der Heijden, I Sanders) pp. 375–413 (Springer-Verlag: Berlin)

Taylor DL, Bruns TD, Szaro TM, Hodges SA (2003) Divergence in mycorrhizal specialization within Hexalectris spicata (Orchidaceae), a nonphotosynthetic desert orchid. American Journal of Botany 90, 1168–1179. open url image1

Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN (2005) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society 84, 1–54.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vallius E (2001) Factors affecting fruit set and seed production in Dactylorhiza maculata (Orchidaceae). Botanical Journal of the Linnean Society 135, 89–95.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wallace LE (2002) Examining the effects of fragmentation on genetic variation in Platanthera leucophaea (Orchidaceae): inferences from allozyme and random amplified polymorphic DNA markers. Plant Species Biology 17, 37–49.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wallace LE (2003) The cost of inbreeding in Platanthera leucophaea (Orchidaceae). American Journal of Botany 90, 235–242. open url image1

Warcup JH (1973) Symbiotic germination of some Australian terrestrial orchids. New Phytologist 72, 387–392.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warcup JH (1988) Mycorrhizal associations of isolates of Sebacina vermifera.  New Phytologist 110, 227–231.
Crossref | GoogleScholarGoogle Scholar | open url image1

Weiss M, Selosse M-A, Rexer K-H, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycological Research 108, 1003–1010.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Whigham DF, O’Neill JP, Rasmussen HN, Caldwell BA, McCormick MK (2006) Seed longevity in terrestrial orchids – potential for persistence in situ seed banks. Biological Conservation 129, 24–30.
Crossref | GoogleScholarGoogle Scholar | open url image1

Willems JH, Dorland E (2000) Flowering frequency and plant performance and their relation to age in the perennial orchid Spiranthes spiralis (L.) Chevall. Plant Biology 2, 344–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

Willems JH, Melser C (1998) Population dynamics and life-history of Coeloglossum virde (L.) Harm.: an endangered orchid species in The Netherlands. Botanical Journal of the Linnean Society 126, 83–89.
Crossref | GoogleScholarGoogle Scholar | open url image1

Willems JH, Balounova Z, Kindlmann P (2001) The effect of experimental shading on seed production and plant survival of Spiranthes spiralis (Orchidaceae). Lindleyana 16, 31–37. open url image1

Wotavová K, Balounová Z, Kindlmann P (2004) Factors affecting persistence of terrestrial orchids in wet meadows and implications for their conservation in a changing agricultural landscape. Biological Conservation 118, 271–279.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zelmer CD, Currah RS (1997) Symbiotic germination of Spiranthes lacera (Orchidaceae) with naturally occurring endophyte. Lindleyana 12, 142–148. open url image1

Zelmer CD, Cuthbertson L, Currah RS (1996) Fungi associated with terrestrial orchid mycorrhizas, seeds and protocorms. Mycoscience 37, 439–448.
Crossref | GoogleScholarGoogle Scholar | open url image1