Colonisation of jarrah forest bauxite-mine rehabilitation areas by orchid mycorrhizal fungi
Margaret Collins A D , Mark Brundrett B , John Koch C and Krishnapillai Sivasithamparam AA School of Earth and Geographical Sciences (Soil Science Discipline), Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, WA 6009, Australia.
B School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, WA 6009, Australia.
C Alcoa World Alumina Australia, Huntly Mine, PO Box 172, Pinjarra, WA 6208, Australia.
D Corresponding author. Email: mcollins@cyllene.uwa.edu.au
Australian Journal of Botany 55(6) 653-664 https://doi.org/10.1071/BT06170
Submitted: 14 August 2006 Accepted: 12 February 2007 Published: 27 September 2007
Abstract
Orchids require mycorrhizal fungi for germination of seed and growth of seedlings. The colonisation of bauxite-mine rehabilitation areas by orchids is therefore dependent on the availability of both seed and mycorrhizal fungi. Orchid mycorrhizal fungi baiting trials were carried out in rehabilitation areas that were 1, 10 and 26 years old (established in 2001, 1992 and 1976) and adjacent unmined jarrah forest areas at Jarrahdale, Western Australia. Fungal baits consisted of buried six-chambered nylon-mesh packets containing seed of six jarrah forest orchid taxa, Caladenia flava subsp. flava R.Br., Disa bracteata Sw., Microtis media subsp. media R.Br., Pterostylis recurva Benth., Pyrorchis nigricans (R.Br.) D.L.Jones & M.A.Clem. and Thelymitra crinita Lindl. Detection of orchid mycorrhizal fungi was infrequent, especially at the youngest rehabilitation sites where only mycorrhizal fungi associated with P. recurva were detected. Mycorrhizal fungi of the other orchid taxa were widespread but sparsely distributed in older rehabilitation and forest areas. Detection of mycorrhizal fungi varied between taxa and baiting sites for the two survey years (2002 and 2004). Caladenia flava subsp. flava and T. crinita mycorrhizal fungi were the most frequently detected. The presence of C. flava mycorrhizal fungi was correlated with leafy litter cover and maximum depth, and soil moisture at the vegetation type scale (50 × 5 m belt transects), as well as tree and litter cover at the microhabitat scale (1-m2 quadrats). The presence of T. crinita mycorrhizal fungi was positively correlated with soil moisture in rehabilitation areas and low shrub cover in forest. The frequency of detection of orchid mycorrhizal fungi both at rehabilitated sites (15–25% of baits) and in unmined forest (15–50% of baits) tended to increase with rehabilitation age as vegetation recovered. The failure of some orchid taxa to reinvade rehabilitation areas is unlikely to be entirely due to absence of the appropriate mycorrhizal fungi. However, since the infrequent detection of fungi suggests that they occur in isolated patches of soil, the majority of dispersed orchid seeds are likely to perish, especially in recently disturbed habitats.
Acknowledgements
This study was funded by an Australian Research Council Linkage grant (LP0221076). We thank Yumiko Bonnardeaux and Richard Cooke who provided valuable assistance with the fieldwork and the environmental research scientists at Alcoa World Alumina Australia Limited for access to information on the Jarrahdale mine site and assistance with the choice of study sites. We also thank Kristian Pollock from the Department of Conservation and Land Management for providing information on planned control burns in the Jarrahdale area.
Arditti J, Ghani AKA
(2000) Tansley Review No. 110: numerical and physical properties of orchid seeds and their biological implications. New Phytologist 145, 367–421.
| Crossref | GoogleScholarGoogle Scholar |
Babich H, Stotzky G
(1978) Toxicity of zinc to fungi, bacteria and coli phages influence of chloride ions. Applied and Environmental Microbiology 36, 906–914.
| PubMed |
Batty AL,
Dixon KW,
Brundrett M, Sivasithamparam K
(2001a) Constraints to symbiotic germination of terrestrial orchid seed in a Mediterranean bushland. New Phytologist 152, 511–520.
| Crossref | GoogleScholarGoogle Scholar |
Batty AL,
Dixon KW,
Brundrett M, Sivasithamparam K
(2001b) Long-term storage of mycorrhizal fungi and seed as a tool for the conservation of endangered Western Australian terrestrial orchids. Australian Journal of Botany 49, 619–628.
| Crossref | GoogleScholarGoogle Scholar |
Bonnardeaux Y,
Brundrett MC,
Batty AL,
Dixon KW,
Koch JM, Sivasithamparam K
(2007) Diversity of mycorrhizal fungi of terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions. Mycological Research 111, 51–61.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brundrett M,
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 |
Carling DE,
Pope EJ,
Brainard KA, Carter DA
(1999) Characterization of mycorrhizal isolates of Rhizoctonia solani from an orchid, including AG-12, a new anastomosis group. Phytopathology 89, 942–946.
| Crossref | GoogleScholarGoogle Scholar |
Clements MA,
Muir H, Cribb PJ
(1986) A preliminary report on the symbiotic germination of European terrestrial orchids. Kew Bulletin 41, 437–445.
Collins MT
(2005) How do you determine when orchid seed germination has been successful? Orchadian 15, 60–71.
Collins MT,
Brundrett M, Sivasithamparam K
(2005) Recovery of orchids in the post-mining landscape. Selbyana 26, 255–264.
Gardner JH, Malajczuk N
(1988) Recolonization of rehabilitated bauxite mine sites in Western Australia by mycorrhizal fungi. Forest Ecology and Management 24, 27–42.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Grant CD, Loneragan WA
(2001) The effects of burning on the understorey composition of rehabilitated bauxite mines in Western Australia: community changes and vegetation succession. Forest Ecology and Management 145, 255–279.
| Crossref | GoogleScholarGoogle Scholar |
Hollick PS,
Taylor RJ,
McComb JA, Dixon KW
(2005) If orchid mycorrhizal fungi are so specific, how do natural hybrids cope? Selbyana 26, 159–170.
Hutton BJ,
Dixon KW,
Sivasithamparam K, Pate JS
(1997) Effect of habitat disturbance on inoculum potential of ericoid endophytes of Western Australian heaths (Epacridaceae). New Phytologist 135, 739–744.
| Crossref | GoogleScholarGoogle Scholar |
Jasper DA,
Abbott LK, Robson AD
(1989a) The loss of VA mycorrhizal infectivity during bauxite mining may limit the growth of Acacia pulchella R.Br. Australian Journal of Botany 37, 33–42.
| Crossref | GoogleScholarGoogle Scholar |
Jasper DA,
Abbott LK, Robson AD
(1989b) Soil disturbance reduced the infectivity of external hyphae of vesicular-arbuscular mycorrhizal fungi. New Phytologist 112, 93–100.
| Crossref | GoogleScholarGoogle Scholar |
Koch JM, Ward SC
(1994) Establishment of understory vegetation for rehabilitation of bauxite-mined areas in the jarrah forest of Western Australia. Journal of Environmental Management 41, 1–15.
| Crossref | GoogleScholarGoogle Scholar |
Masuhara G, Katsuya K
(1994) In situ and in vitro specificity between Rhizoctonia spp. and Spiranthes sinensis (Persoon) Ames. var. amoena (M.Bieberstein) Hara (Orchidaceae). New Phytologist 127, 711–718.
| Crossref | GoogleScholarGoogle Scholar |
Masuhara G,
Neate SM, Schisler DA
(1994) Characteristics of some Rhizoctonia spp. from South Australian plant nurseries. Mycological Research 98, 83–87.
McKendrick SL,
Leake JR,
Taylor DL, Read DJ
(2002) Symbiotic germination and development of the myco-heterotrophic orchid Neottia nidus-avis in nature and its requirement for locally distributed Sebacina spp. New Phytologist 154, 233–247.
| Crossref | GoogleScholarGoogle Scholar |
McQuaker NR,
Brown DF, Kluckner PD
(1979) Digestion of environmental materials for analysis by inductively coupled plasma-atomic emission spectrometry. Analytical Chemistry 51, 1082–1084.
| Crossref | GoogleScholarGoogle Scholar |
Muir BG
(1977) Biological survey of the Western Australian wheatbelt, part II. Records of the Western Australian Museum , 1–24.
Murren CJ, Ellison AM
(1998) Seed dispersal characteristics of Brassavola nodosa (Orchidaceae). American Journal of Botany 85, 675–680.
| Crossref | GoogleScholarGoogle Scholar |
O’Connell AM
(1986) Effect of understorey on decomposition and nutrient content of eucalypt forest litter. Plant and Soil 92, 235–248.
| Crossref | GoogleScholarGoogle Scholar |
O’Connell AM, Menage P
(1983) Decomposition of litter from 3 major plant species of jarrah Eucalyptus-marginata forest in relation to site fire history and soil type. Australian Journal of Ecology 8, 277–286.
Otero JT,
Ackerman JD, Bayman P
(2004) Differences in mycorrhizal preferences between two tropical orchids. Molecular Ecology 13, 2393–2404.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Perkins AJ,
Masuhara G, McGee PA
(1995) Specificity of the associations between Microtis parviflora (Orchidaceae) and its mycorrhizal fungi. Australian Journal of Botany 43, 85–91.
| Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Ramsey RR,
Dixon KW, Sivasithamparam K
(1986) Patterns of infection and endophytes associated with Western Australian orchids. Lindleyana 1, 203–214.
Rasmussen HN
(2002) Recent developments in the study of orchid mycorrhiza. Plant and Soil 244, 149–163.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Rasmussen HN, Whigham DF
(1998) Importance of woody debris in seed germinaton of Tipularia discolor (Orchidaceae). American Journal of Botany 85, 829–834.
| Crossref | GoogleScholarGoogle Scholar |
Selosse M-A,
Weiss M,
Jany J-L, Tillier A
(2002a) Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) L.C.M.Rich. and neighbouring tree ectomycorrhizae. Molecular Ecology 11, 1831–1844.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Selosse MA,
Bauer R, Moyersoen B
(2002b) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. New Phytologist 155, 183–195.
| Crossref | GoogleScholarGoogle Scholar |
Siddiqui IA,
Shaukat SS, Hamid M
(2002) Role of zinc in rhizobacteria-mediated suppression of root-infecting fungi and root-knot nematode. Journal of Phytopathology (Berlin) 150, 569–575.
| Crossref | GoogleScholarGoogle Scholar |
Streeter TC,
Rengel Z,
Neate SM, Graham RD
(2001) Zinc fertilisation increases tolerance to Rhizoctonia solani (AG 8) in Medicago truncatula. Plant and Soil 228, 233–242.
| Crossref | GoogleScholarGoogle Scholar |
Sweeney RA, Rexroad PR
(1987) Comparison of Leco-FP-228 nitrogen determinator with AOAC copper catalyst Kjeldahl method for crude protein. Journal of the Association of Official Analytical Chemists 70, 1028–1030.
Thongbai P,
Graham RD,
Neate SM, Webb MJ
(1993a) Interaction between zinc nutritional status of cereals and Rhizoctonia root rot severity. II. Effect of Zn on disease severity of wheat under controlled conditions. Plant and Soil 153, 215–222.
| Crossref | GoogleScholarGoogle Scholar |
Thongbai P,
Hannam RJ,
Graham RD, Webb MJ
(1993b) Interaction between zinc nutritional status of cereals and Rhizoctonia root rot severity. I. Field observations. Plant and Soil 153, 207–214.
| Crossref | GoogleScholarGoogle Scholar |
van der Kinderen G
(1995) A method for the study of field germinated seeds of terrestrial orchids. Lindleyana 10, 68–73.
Warcup JH
(1971) Specificity of mycorrhizal association in some Australian terrestrial orchids. New Phytologist 70, 41–46.
| Crossref | GoogleScholarGoogle Scholar |
Warcup JH
(1981) The mycorrhizal relationships of Australian orchids. New Phytologist 87, 371–381.
| Crossref | GoogleScholarGoogle Scholar |
Ward SC
(2000) Soil development on rehabilitated bauxite mines in south-west Australia. Australian Journal of Soil Research 38, 453–464.
| Crossref | GoogleScholarGoogle Scholar |
Zall DM,
Fisher D and
Garner MQ
(1956)
Soil development on rehabilitated bauxite mines in south-west Australia.
Analytical Chemistry Vol. 28, 1665–1668.
Zettler LW, Hofer CJ
(1998) Propagation of the little club-spur orchid (Platanthera clavellata) by symbiotic seed germination and its ecological implications. Environmental and Experimental Botany 39, 189–195.
| Crossref | GoogleScholarGoogle Scholar |