Recovery of terrestrial orchids in the post-mining landscape

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Selbyana 25(2): 000–000. 2004.

RECOVERY OF TERRESTRIAL ORCHIDS IN THE

POST-MINING LANDSCAPE

MARGARET COLLINS*

School of Earth and Geographical Sciences (Soil Science Discipline), Faculty of Natural andAgricultural Sciences, The University of Western Australia, Crawley, WA 6009 Australia.

Email: [email protected]

JOHN KOCH

Alcoa World Alumina Australia, P.O. Box 252, Applecross, WA 6953 Australia.

MARK BRUNDRETT

School of Plant Sciences, Faculty of Natural and Agricultural Sciences, The University ofWestern Australia, Crawley, WA 6009 Australia.

KRISHNAPILLAI SIVASITHAMPARAM

School of Earth and Geographical Sciences (Soil Science Discipline), Faculty of Natural andAgricultural Sciences, The University of Western Australia, Crawley, WA 6009 Australia.

ABSTRACT. Currently, Alcoa World Alumina Australia mines and rehabilitates ca. 550 ha of jarrah foresteach year at two open-cut bauxite mines in Western Australia. The aim of Alcoa’s rehabilitation programis to re-establish a functional and self-sustaining jarrah forest ecosystem in these mined areas. Many in-digenous geophytic plant species, however, fail to re-establish or do so very slowly. Indigenous terrestrialorchids form a significant proportion of the species difficult to re-establish. The dominant source of orchidpropagules within the rehabilitation areas is wind-dispersed seed. Recruitment of new plants is dependenton availability of both viable seed and appropriate mycorrhizal fungi in the soil of suitable microhabitatsat the beginning of the wet season. Flora surveys were undertaken to determine orchid species and theirdensity in a temporal sequence of rehabilitation areas, so as to establish the sequence of species recovery.Total orchid population and clonal orchids were found to have returned to rehabilitation areas within 5years at densities not significantly different from those of adjacent unmined forest. Numbers of total speciesand clonal species also were found to have returned to rehabilitation areas within 5 years at densities notsignificantly different from those of adjacent unmined forest. Orchid species identified as disturbance op-portunists returned to rehabilitation areas within 5 years with densities increasing during the following 10years but dropping to numbers not significantly different from those of adjacent unmined forest after 25years. No disturbance opportunists were found in any unmined forest. Future studies will investigate therecovery of selected individual species in rehabilitation areas, vegetation associations of these species inboth unmined forest and rehabilitation areas, and the diversity of their mycorrhizal fungi.

Key words: terrestrial orchids, jarrah forest, mining rehabilitation

INTRODUCTION

The southwest botanical province of WesternAustralia is known for its high floristic biodi-versity. The two major forest ecosystems occur-ring within this floristic province are karri (Eu-calyptus diversicolor F.Muell.) and jarrah (Eu-calyptus marginata Donn ex Smith) forests (FIG-URE 1). Karri forest is limited to high rainfallareas of the lower southwest. Jarrah forest is de-limited by the Darling Scarp in the west, the750-mm isohyet in the east (the limit of mallet-wandoo woodlands in the north and marri-wan-doo woodlands in the south), and the climatic

* Corresponding author.

boundary between dry and more moderate Med-iterranean climates in the south (Beard 1990).Jarrah forest is divided into northern and south-ern sub-regions along a poorly defined line,where ironstone gravels become less prevalent,and understory flora become more like that ofthe karri forest (Beard 1990). Alcoa World Alu-mina Australia, which was first granted the min-ing lease to the northern jarrah forest of south-west Western Australia in 1961, has been miningbauxite since 1963 at three open-cut mine sites(FIGURE 1). Currently, the company mines andrehabilitates ca. 550 ha of jarrah forest each yearat the Huntly and Willowdale mine sites. Thethird mine at Jarrahdale, which operated 1963–1998, has been rehabilitated and decommis-

Volume 25(2) 2004SELBYANA



FIGURE 1. Southwest region of Western Australia showing extent of an Alcoa mining lease in relation tojarrah and karri forests.

sioned. Originally the aim of rehabilitation wasto establish vegetation cover as quickly as pos-sible, often using fast-growing exotic species ornon-indigenous Australian species. During the

period of the lease, Alcoa has adopted a processof continuous improvement in its environmentalmanagement and mine-rehabilitation standards.The present aim of rehabilitation is to re-estab-

COLLINS ET AL.: ORCHIDS IN POST-MINING LANDSCAPES



lish a functional and self-sustaining jarrah forestecosystem in areas that have been mined forbauxite (Elliott et al. 1996). This means re-es-tablishing, as near as is practicable, the pre-min-ing vegetation structure, species diversity, andforest function.

Many indigenous geophytic plant species ei-ther fail to re-establish or do so very slowlywithin rehabilitation areas (Koch & Ward 1994,Koch et al. 1996, Grant & Koch, 2003). Terres-trial orchids represent ca. 20% of difficult to re-establish species. The recovery of orchids inmine rehabilitation areas has been expected tooccur through the natural dispersal of seed fromsurrounding unmined forest. Orchid seed, mi-nute and naturally dispersed by wind, has beenknown to travel substantial distances. Reports ofdistances greater than 100 km have been madein several instances (Rasmussen 1995). The or-chid flora of the southwest botanical provinceranks among the most diverse terrestrial orchidfloras in the world with more than 340 taxa iden-tified (Hoffman & Brown 1998). At least 73 ofthese taxa have been found within the jarrah for-est (A. Brown pers. comm.). All but one of theseindigenous orchids are terrestrial, tuberous, sum-mer deciduous, and mycorrhizal. The exception,Cryptostylis ovata (R.Br.), also is terrestrial, tu-berous, and mycorrhizal but evergreen. Orchidmycorrhizal fungi are required for the germina-tion of seed and for nearly the complete nutritionof protocorms and seedlings up to the develop-ment of photosynthetic capacity. Generally my-corrhizal relationships are regarded as symbiot-ic, in the sense that they are mutualistic, withboth partners deriving benefits from the relation-ship (Johnson et al. 1997). Orchid mycorrhizalrelationships are atypical, as nutrient flow isthought to be unidirectional—-from fungus toplant (Gebauer & Meyer 2003, Smith & Read1997). The degree of dependence on mycorrhi-zal fungus and the specificity of this relationshipmay be variable, with some terrestrial orchidspecies regarded as particularly vulnerable to en-vironmental disturbance because of their depen-dence on a highly specific fungus (this is espe-cially true for achlorophyllous species) (Matsu-hara & Katsuka 1994, Andersen & Rasmussen1996, Perkins et al. 1995).

Soil disturbance is known to reduce the in-oculum potential of soil fungi through disruptionof the hyphal network and subsequent loss ofinfectivity (Hutton et al. 1997, Jasper et al.1989a, 1989b). The stripping and respreading oftopsoil in bauxite mining causes severe disrup-tion of the hyphal network and therefore greatlyreduces the inoculum potential of orchid mycor-rhizal fungi. Recruitment of new plants in bush-land is dependent on availability of both viable

seed and the appropriate mycorrhizal fungi inthe soil of suitable microhabitats at the begin-ning of the wet season. Low recruitment ratesfrom natural seed dispersal observed in bushlandin Western Australia may be the result of thepatchy distribution of the mycorrhizal fungi inthe soil and the scarcity of suitable microhabitatsin the landscape (Batty et al. 2001, McKendricket al. 2002). Establishment of orchids in reha-bilitation areas requires the availability of viableseed, recovery of the inoculum potential of my-corrhizal fungi, and establishment of suitablemicrohabitats through the regrowth of vegeta-tion.

The aim of this project is to examine a tem-poral sequence of bauxite mine rehabilitation ar-eas and adjacent unmined areas of jarrah forestto determine the diversity and frequency of oc-currence of terrestrial orchids in both. Prelimi-nary results are presented in this paper.

MATERIALS AND METHODS

The Jarrahdale bauxite mine is located alongthe Darling Scarp near the town of Jarrahdale,55 km southeast of Perth in Western Australia.The climate is dry Mediterranean with a meanannual rainfall of 1220 mm during the winter-wet season. Mining commenced at Jarrahdale in1963, and the region was actively mined until1998; rehabilitation was completed in 2001, andthe site was decommissioned in 2002. In thebauxite mining process, large earth-movingequipment removes the soil covering the bauxiteas two layers, topsoil (depth 10–15 cm) andoverburden (depth 15–50 cm). The overburdenis stockpiled next to the pit, and the topsoil isused for direct return at another site to minimizeloss of propagules of both plants and mycorrhi-zal fungi. After removal of the bauxite layer (2–5 m depth), the pit is rehabilitated. In the post-mining rehabilitation process, pit walls are bat-tered down, and the pit is landscaped. Overbur-den and topsoil then are respread in the correctorder, and the area is ripped (to a 1.5-m depth),seeded, and fertilized. The current seeding mix-ture contains seed of the two dominant tree spe-cies—-Eucalyptus marginata (jarrah) and Cor-ymbia calophylla (Lindl.) K.D.Hill &L.A.S.Johnson (marri)—-along with more than60 understory species (Nichols et al. 1991).

Both the seeding mix and the soil seed bankin respread topsoil are valuable sources of prop-agules for revegetation of many plant species.Orchid seed, however, has never been added tothe seed mixtures used for revegetation. Becausethe orchid soil seed bank in southwest WesternAustralia is known to be short-lived (Batty et al.




2000), respread topsoil is not likely to be a sig-nificant source of viable orchid propagules.

Orchid Survey

Single-belt transects (5 m by 50 m), each con-sisting of ten contiguous 5 m 3 5 m quadrats,were established in four replicates of 1-, 5-, 10-,and 15-year-old rehabilitation areas (establishedin 2001, 1997, 1992, and 1987 respectively) andin adjacent unmined forest at Jarrahdale, West-ern Australia, in autumn 2002. Additionally, twotransects were established in 27-year-old reha-bilitation areas with an overstory of marri, anda single transect was established in a 26-year-old rehabilitation area; each was paired withtransects in adjacent unmined forest. These threetransects are identified as .25-year-old rehabil-itation areas. Two transects also were establishedthrough populations of Cryptostylis ovata in theunmined forest (a total of 40 transects). Eachtransect was scored for the number of orchidspecies present and number of plants of eachspecies in each quadrat during the 2002 growingseason. Data also were collected on surroundingvegetation cover and structure, plant species pre-sent, and litter cover.

Data Analyses

All data were analyzed using GenStat Version7, Lawes Agricultural Trust, Rothamsted Exper-imental Station.

RESULTS

Orchids were found to have re-established inall rehabilitation areas except the 1-year-old re-habilitation areas (established 2001). The oldesttransects had the highest mean density of or-chids (FIGURE 2A); however, this only was sig-nificantly different (at P # 0.05) from 1- and 5-year-old rehabilitation areas. The orchid densityof 1-year-old rehabilitation areas was signifi-cantly less than all other age categories. Orchiddensity in unmined forest was highly variable;and, despite large differences in the mean den-sity of orchids, none of the forested areas dif-fered significantly from each other or from theiradjacent rehabilitation areas.

The mean number of orchid species presentfor 1-year-old rehabilitation areas was signifi-cantly different (at P # 0.05) from all other re-habilitation areas and forest transects (FIGURE

3A). The mean numbers of species in forest ad-jacent to the .25- and 5-year-old rehabilitationareas differed significantly from each other butnot from other forested areas or from their ad-jacent rehabilitation areas.

As neither orchid density nor species numberrevealed significant changes with time past 5years, the data for clonal orchids was examinedseparately. The mean density of clonal orchidsfor .25-year-old rehabilitation areas differedsignificantly (at P # 0.05) from all other reha-bilitation areas and forested areas, except forthose adjacent to 15- and .25-year-old rehabil-itation areas. These forested areas, however, didnot differ significantly from the rehabilitation ar-eas or other forested areas (FIGURE 2B).

The mean number of clonal orchid species(FIGURE 3B) in 1-year-old rehabilitation areaswas significantly lower than in all other rehabil-itation and forested areas (at P # 0.05), but thenumber of clonal species did not differ signifi-cantly from adjacent forested areas. The 15- and.25-year-old rehabilitation areas had a highermean number of species present but differed sig-nificantly only from the 1-year-old rehabilitationarea and its adjacent forest.

Orchid species identified as disturbance op-portunists were scored for all age rehabilitationareas and forest. The mean number of distur-bance opportunists (FIGURE 3C) in rehabilitationareas that were 1, 5, and .25 years old weresignificantly lower than in 10- and 15-year-oldrehabilitation areas (at P # 0.05). No distur-bance opportunists were found in any of the for-est sites.

DISCUSSION

The recovery of flora in post-bauxite miningrehabilitation areas may well follow the ‘‘initialfloristic composition’’ model (Koch & Ward1994, Grant & Loneragan 2001), that is, the flo-ra composition immediately following distur-bance determines future shifts in dominance. Inthe post-mining landscape, the initial composi-tion is determined by the composition of boththe seeding mixture and the soil seed bank inrespread topsoil. Alcoa’s rehabilitation proce-dures originally consisted of planting exotic treespecies (e.g., Pinus pinaster) but were latermodified to seeding with mostly leguminous un-derstory species and non-indigenous eucalypts(e.g., Eucalyptus resinifera). More recently, re-habilitation areas have been seeded with indig-enous tree species and a broader range of un-derstory species and then planted with tissue-cultured recalcitrant taxa (Grant & Koch 2003).Orchid seed, however, has never been includedin seeding mixtures, and the soil seed bank isnot expected to provide viable propagules (Battyet al. 2000). Orchids therefore are not expectedto re-establish rapidly.

Natural recruitment of terrestrial orchids islow compared to the number of seeds they pro-




FIGURE 2. Mean number of orchid species found in a temporal sequence of transects in rehabilitation areasand adjacent unmined forest. For 1-, 5-, 10-, and 15-year-old rehabilitation areas, n 5 4; for .25-year-old areas,n 5 3. A. All orchid species. B. Clonal orchid species. Transect area 0.025 ha (5 m 3 50 m). Vertical barsrepresent SE (standard error). Columns identified by the same letter are not significantly different.




FIGURE 3. Mean density of orchids (plants ha21) found in a temporal sequence of transects in rehabilitationareas and adjacent unmined forest. For 1-, 5-, 10-, and 15-year-old rehabilitation areas, n 5 4; for .25-year-oldareas, n 5 3. A. All orchids. B. Clonal orchids. C. Disturbance opportunists. Vertical bars represent SE. Columnsidentified by the same letter are not significantly different.

duce (5000–30,000 seeds/pod) (M. Collins un-publ. data, Batty 2001). Recruitment in rehabil-itation areas will be dependent on seed set in thesurrounding forest, adequate dispersal, and therecovery of soil microflora with the progressivebuild up of organic matter. The survey resultsindicate that orchids re-establish in mined areaswithin 5 years in numbers that are not signifi-cantly different from those in unmined forest.Because of the dependence of terrestrial orchidson their mycorrhizal fungi for germination ofseed, nutrition of protocorms, and developmentof adult plants, their presence may be regardedas an indicator of the recovery of their mycor-rhizal fungi in the soil environment. Orchid my-corrhizal partners—-rhizoctonia-like fungi pri-marily found in the coarse fraction of soil or-ganic matter (partially decomposed litter) (Brun-drett et al. 2003)—-are expected to occur early

in the succession of species in the recovery ofsoil microflora.

The recovery of orchids with differing growthhabits will influence the future diversity andpopulation size of orchids within the rehabilita-tion areas. Clonal orchids increase populationsize quickly because of their primarily vegeta-tive reproductive strategy. These species, absentfrom 1-year-old rehabilitation areas, were pre-sent in 5-year-old and older areas. In the forests,Grant and Koch (2003) found that the highestdensities of any indigenous orchids were ofclonal species (TABLE 1). These species re-estab-lished in rehabilitation areas with densitiesreaching ca. 10% that of unmined forest in the.10-year-old rehabilitation area. Other species(except disturbance opportunists) generally werepresent as a much lower percentage of the pre-mining density. Considerable time, probably




TABLE 1. Mean density of orchids (plants ha21) found in permanent vegetation monitoring plots by Alcoa,adapted from Grant and Koch (2003). Species have been separated by growth habit and sorted by decreasingforest density. Species names in bold are absent from either rehabilitation areas or forest. A single asterisk(*) refers to weed species, and a double asterisk (**) refers to an indigeneous species not normally foundin jarrah forest.

Orchid species

Scientific name Common name

Mean density (no./ha21)

Forest All rehab .10 yr old

Clonal speciesCyrtostylis robustaCaladenia flavaPterostylis nanaLeporella fimbriaPterostylis vittata

Mosquito orchidCowslip orchidSlender snail orchidHare orchidBanded greenhood

3515.82870.52694.8

607.0520.3

0.2138.5133.3

0.460.5

0.0271.0250.0

0.0119.3

Caladenia reptansCryptostylis ovataMicrotis media

Little pink fairy orchidSlipper orchidCommon mignonette orchid

129.546.2

3.4

1.40.0

889.5

2.30.0

1742.7

Other speciesThelymitra crinitaEriochilus dilatatusThelymitra macrophyllaPyrochis nigricansPterostylis recurvaDisa bracteata*

Blue lady orchidCommon bunny orchidScented sun orchidRed beaksJug orchidSouth African orchid

1183.6709.6399.8237.6171.241.7

1.52.70.4

21.317.6

210.4

3.15.00.8

42.034.8

336.6Cyanicula sericeaPrasophyllum elatumPterostylis barbataPrasophyllum browniiCaladenia macrostylis

Silky blue orchidTall leek orchidDwarf bird orchidChristmas leek orchidLeaping spider orchid

22.520.316.915.813.5

0.20.00.80.2

17.6

0.40.00.00.0

28.7Lyperanthus serratusElythranthera brunonisDiuris carinata**

Rattle beaksPurple enamel orchidTall bee orchid

11.32.30.0

0.00.41.2

0.00.82.3

several decades, will need to elapse for popula-tions of many orchid taxa to reach pre-miningdensities and for diversity to be re-established(FIGURE 4).

The species data of Grant and Koch (2003)were grouped so as to separate species into thefollowing categories: clonal species, disturbanceopportunists, exotic species, and other species.The proportion of species in each category iscompared with those of the current study in TA-BLE 2. The results of each study were generallysimilar for each species category, with the ex-ception that the current study found no exoticspecies in forest sites. This may be an artifactof the current study’s reduced sampling area, orthese species may be responding to forest dis-turbance from causes other than mining in theearlier study.

Three species were identified as disturbanceopportunists from a study of long-term vegeta-tion survey work by Grant and Koch (2003):Microtis media (R.Br.), Disa bracteata (Sw.),and Caladenia macrostylis (R. Fitzg.). We founddisturbance opportunists most abundant in 10-and 15-year-old rehabilitation areas, but densitydropped dramatically in older sites. Bonnar-

deaux presented work at the IOCCII that showeda high diversity of fungal endophytes formingmycorrhiza with D. bracteata (synonym Mona-denia bracteata). This naturalized South Africanspecies is among the most common of the dis-turbance opportunists in the rehabilitated areas.The ability to form mycorrhiza with diverse fun-gi may be advantageous in early recovery of flo-ra. Other edaphic qualities or vegetation struc-tural elements present only in young rehabilita-tion areas may provide a conducive environmentfor these species, e.g., low soil organic matter,intense shade, and lack of competition. Theecology of D. bracteata and other disturbanceopportunists needs to be examined further to de-termine if this species has the potential to beutilized as an indicator species in the progressof vegetation recovery.

At present, we are examining the relationshipbetween age of rehabilitation area and density ofselected individual species. Future work is di-rected to several areas; firstly, we are examiningthe vegetation structure and species diversity as-sociated with the occurrence of individual orchidspecies in rehabilitation areas and unmined for-est. We also have carried out seed-baiting ex-




FIGURE 4. Native orchid habitat and species in southwest region of Western Australia. A. Un-mined jarrahforest. B, C. Slipper orchid (Cryptostylis ovata). D. Cowslip orchid (Caladenia flava). E. Blue lady orchid(Thelymitra crinita). F. South African orchid (Disa bracteata).




TABLE 2. Comparison of the number of orchid species of differing growth strategies found in the Alcoaretrospective study (Grant & Koch 2003) with data from the current project.

Orchid species category

Alcoa survey


Current study


No. spp.ClonalDisturbance opportunistsExotic speciesOther species

TotalTotal area surveyed (ha)

930

1022

4.44

8318

2025.88

6316

1613.08

6008

140.55

6315

150.45

6314

140.175

periments to determine the presence or absenceof appropriate mycorrhizal fungi in the topsoilof both forest and rehabilitation areas, and willbe examining the diversity of fungal endophytesassociated with selected orchid species.

ACKNOWLEDGMENTS

This study was funded by an Australian Re-search Council Linkage grant (LP0221076). Wethank the environmental research scientists atAlcoa World Alumina Australia Limited for ac-cess to the results of long-term vegetation mon-itoring and information on the field sites.

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Recovery of terrestrial orchids in the post-mining landscape