Root morphology, photosynthesis, water relations and development of
jarrah (Eucalyptus marginata) in response to soil constraints at
restored bauxite mines in south-western Australia
Christopher Szota B.Sc. (Hons)
This thesis is presented for the degree of
Doctor of Philosophy
of the University of Western Australia
School of Plant Biology
November 2009
i
Summary Bauxite mining is a major activity in the jarrah (Eucalyptus marginata Donn ex Sm.)
forest of south-western Australia. After mining, poor tree growth can occur in some
areas. This thesis aimed to determine whether soil constraints, including reduced depth
and compaction, were responsible for poor tree growth at low-quality restored bauxite
mines. In particular, this study determined the response of jarrah root morphology, leaf-
scale physiology and growth/development to soil constraints at two contrasting (low-
quality and high-quality) restored bauxite-mine sites.
Jarrah root excavations at a low-quality restored site revealed that deep-ripping
equipment failed to penetrate the cemented lateritic subsoil, causing coarse roots to be
restricted to the top 0.5 m of the soil profile, resulting in fewer and smaller jarrah trees.
An adjacent area within the same mine pit (high-quality site) had a kaolinitic clay
subsoil, which coarse roots were able to penetrate to the average ripping depth of 1.5 m.
Impenetrable subsoil prevented development of taproots at the low-quality site, with
trees instead producing multiple lateral and sinker roots. Trees in riplines, made by
deep-ripping, at the high-quality site accessed the subsoil via a major taproot, while
those on crests developed large lateral and sinker roots.
The influence of soil constraints on the physiology of jarrah and co-occurring
marri (Corymbia calophylla Lindl.) at the low- and high-quality restored bauxite-mine
sites was also studied. Impenetrable subsoil at the low-quality site resulted in fewer,
smaller trees compared with the high-quality site. Restriction of root systems at the
low-quality site significantly reduced morning stomatal conductance, photosynthesis,
midday leaf water potential and average daily leaf relative water content in both species
during drought; this explains the difference in above-ground productivity between sites.
Jarrah showed cell-wall elastic adjustment during drought which was associated with
higher stomatal conductance and lower water status compared with marri. Marri
maintained lower stomatal conductance and higher water status during drought,
suggesting that it uses water more conservatively than jarrah, and may therefore be
better suited to surviving extended periods of drought. Leaves of marri osmotically
adjusted during drought which may explain its ability to maintain higher water status
compared with jarrah.
This study applied tree-ring analysis to describe when stress began to affect
above-ground growth of jarrah at two contrasting restored bauxite-mine sites. Trees at
ii
the low-quality site showed slow diameter growth rates from establishment onwards,
presumably as a result of root system restriction. At the high-quality site, trees unable
to access the subsoil with their taproot showed slow initial development prior to a boost
in growth, most likely related to time taken for sinker roots to access the subsoil. Trees
on crests at the high-quality site had slower diameter growth rates than those in riplines,
possibly due to trees in riplines capturing a greater resource pool compared with trees
on crests. Tree-ring width was positively correlated with rainfall received from summer
to autumn prior to initiation of diameter growth for trees at the low-quality site.
Conversely, at the high-quality site, trees showed a strong positive correlation between
ring width and rainfall received from autumn to spring during the diameter growth
phase. Higher responsiveness to rainfall received early, as opposed to mid-late in the
growing season, suggests the low soil moisture-storage capacity at the low-quality site
was maximised early in the growing season and therefore additional rainfall did not
increase diameter growth.
Clearly, soil constraints reduced access to stored soil water and were responsible
for poor growth in low-quality restored bauxite mine sites. These results have key
implications for bauxite-mine-site restoration in south-western Australia. Firstly,
despite jarrah producing a range of roots, access to the subsoil via deep-ripping must be
facilitated in order to prevent exposure of trees to damaging water deficits. Secondly,
marri clearly demonstrates different drought-response mechanisms compared with
jarrah, making it a significant component of the jarrah forest. Marri has an enhanced
potential to survive sites where water availability is low or highly variable, as it uses
water more conservatively than jarrah. Thirdly, evidence presented in this thesis
indicates that trees on crests rather than riplines should be preferentially thinned at
overstocked restored sites, as they have lower growth potential and sub-optimal root
systems.
iii
Table of contents Summary ................................................................................................................................ i Table of contents ................................................................................................................. iii Acknowledgements .............................................................................................................. vi Declaration of originality .................................................................................................. viii General introduction ........................................................................................................... 1 Introduction ........................................................................................................................... 1 The jarrah forest region ......................................................................................................... 2 Bauxite mining in the jarrah forest......................................................................................... 4 Morphological, physiological and developmental responses to drought .............................. 7
Root morphology and drought ................................................................................... 7 Physiological mechanisms and drought .................................................................. 11 Growth and development in response to drought .................................................... 18
Thesis outline ....................................................................................................................... 20 Chapter One ............................................................................................................. 20 Chapter Two ............................................................................................................ 20 Chapter Three .......................................................................................................... 21 Concluding discussion ............................................................................................ 21
References ............................................................................................................................ 21 Chapter 1: Root morphology of jarrah (Eucalyptus marginata) trees in relation to post-mining deep-ripping in south-western Australia .................................................... 31 Abstract ................................................................................................................................ 31 Introduction ......................................................................................................................... 31 Materials and Methods ........................................................................................................ 33
Study site ................................................................................................................. 33 Stand characteristics ................................................................................................ 34 Soil texture and bulk density ................................................................................... 34 Tree root morphology ............................................................................................. 36 Root cross-sectional area allocation calculations .................................................... 36 Data analyses ........................................................................................................... 37
Results ................................................................................................................................. 37 Stand characteristics ................................................................................................ 37 Soil texture, gravel content and bulk density .......................................................... 38 Taproot and sinker root depth ................................................................................. 39 Root number and location ....................................................................................... 40 Root size .................................................................................................................. 41 Allocation to root type ............................................................................................. 42
Discussion ........................................................................................................................... 44 Tree productivity as a function of soil texture, deep-ripping and coarse root depth ........................................................................................................................ 44 Tree root distribution in response to soil texture and deep-ripping ......................... 45
Conclusions ......................................................................................................................... 47 References ........................................................................................................................... 47
iv
Chapter 2. Physiological and stand-level responses of jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) to seasonal drought at low- and high-quality restored bauxite-mine sites in south-western Australia .................................... 52 Abstract ............................................................................................................................... 52 Introduction ......................................................................................................................... 52 Materials and Methods ........................................................................................................ 55
Study site ................................................................................................................. 55 Weather data............................................................................................................. 55 Stand characteristics ................................................................................................ 55 Study tree selection for physiological measurements ............................................. 56 Leaf stomatal conductance and photosynthesis ...................................................... 57 Leaf water potential, osmotic potential and relative water content ......................... 58 Pressure-volume curves ........................................................................................... 59 Data analyses ........................................................................................................... 59
Results ................................................................................................................................. 60 Stand characteristics ................................................................................................ 60 Seasonal patterns of leaf stomatal conductance and photosynthesis ....................... 60 Seasonal patterns of leaf water potential, osmotic potential and relative water content ...................................................................................................................... 62 Stomatal sensitivity in relation to vapour pressure deficit, leaf water potential and relative water content ....................................................................................... 66 Pressure-volume analysis ........................................................................................ 66
Discussion ............................................................................................................................ 70 Key physiological differences between low- and high-quality restored sites ......... 70 Key physiological differences between species in response to site conditions ....... 72
Conclusions ......................................................................................................................... 76 References ........................................................................................................................... 76 Chapter 3. Growth patterns of 13-year-old jarrah (Eucalyptus marginata) at restored bauxite mine sites in south-western Australia as described by tree-ring analysis ............................................................................................................................... 84 Abstract ............................................................................................................................... 84 Introduction ......................................................................................................................... 84 Materials and Methods ........................................................................................................ 87
Study site ................................................................................................................. 87 Weather data ............................................................................................................ 87 Stand characteristics ................................................................................................ 88 Billet preparation ..................................................................................................... 88 Data analyses ........................................................................................................... 90
Results ................................................................................................................................. 91 Stand characteristics ................................................................................................ 91 Annual tree-ring patterns (1992-2004)..................................................................... 91 Relationships between tree size and stand density ................................................... 93 Tree-ring width and climate .................................................................................... 94
Discussion ........................................................................................................................... 96 Tree-ring patterns and stand development .............................................................. 96 Tree-ring patterns and climate .............................................................................. 100
Conclusions ....................................................................................................................... 102 References ......................................................................................................................... 102
v
Concluding discussion ..................................................................................................... 109 Major findings ................................................................................................................... 109 Implications for mine-site restoration ............................................................................... 112 Study limitations and future research ................................................................................ 113 References ......................................................................................................................... 115
vi
Acknowledgements I gratefully acknowledge the funding support of the Australian Research Council and
Alcoa World Alumina Australia.
I would like to thank my supervisors: Erik Veneklaas, Hans Lambers and John
Koch for their knowledge, support, and most importantly, patience over the duration of
my PhD studies.
Many thanks are extended to Claire Farrell, Greg Cawthray and Alasdair Grigg
for assistance with excavation of root systems. Thanks also go to Faron Mengler, Geoff
Kew and Claire Farrell for their comments on an earlier version of Chapter One. I also
extend many thanks to David Bell for his significant improvements to the published
paper based on Chapter One.
The substantial contribution made by Claire Farrell in the field and laboratory
over the course of the physiology study (Chapter 2) is gratefully acknowledged.
Particular thanks are extended to Greg Cawthray for taking the time to teach me how to
operate and repair the Li-6400. The high quality of the physiology dataset is directly
attributable to Greg teaching me how to correctly calibrate and use the system. I also
extend many thanks to Andrew Merchant, Claire Farrell and Dan Wildy for their
comments on Chapter Two.
Thanks to Gabor Szota for assistance with falling and processing the study trees
and to Stephen and Elizabeth Farrell for assistance with preparing tree-ring samples for
analysis (Chapter 3).
Thank you to Gary Cass and Elizabeth Halladin for all your advice on
everything technical. Thanks for your generosity in allowing me to use the laboratory.
Many thanks for every time you gambled by lending me equipment.
Thanks to the Environmental Department at Alcoa World Alumina Australia,
particularly to Ian Colquhoun, for organising student presentation days and getting
students in touch with a wider range of university and industry researchers.
I extend many thanks to Sean Baker, for all the good times, and for your
friendship and support throughout my time at UWA.
Thanks to Alasdair Grigg, Mike Shane, Patrick Mitchell and Imran Malik for
their company and support in the office. Special thanks to Mike for improving my
knowledge of plant physiology and sharpening my glasshouse skills. Thanks to
vii
Alasdair Grigg for your support and good humour over the long haul. Many thanks to
Aleida Williams for your friendship, good cheer and unique baking skills.
Thanks to my family for all their love and support during my time at UWA.
Thanks to my sister, Victoria, for your company and support and for introducing me to
university life. It would not have been possible for me to study up in Perth without the
support of my parents, Gabor and Patricia. Thank you both for your love and for your
faith in me. Many thanks also to Stephen and Elizabeth Farrell for your love and
support and for welcoming me into your family.
I’d like to give special thanks to Justine Edwards at Great Southern Limited,
who has been hugely supportive of me finishing my thesis since I started work in
Albany. I’d also like to thank the plantation foresters down in Albany who have
patiently taught me the trade and whose teachings have largely improved how this thesis
has come together, particularly Bob Edwards, Neville Waugh, Mark Giblett, Peter
English and Galvin Williss.
The last and most important person to give thanks to is my wife, Claire Farrell.
Thanks for your patient teaching, company and hard work out in the often unpleasant
Dwellingup weather. Thanks for your encouragement, love and patience, particularly
over the last 3 years since we moved to sunny Albany.
viii
Declaration of Originality
This thesis is my own work and does not contain information that has been generated by
persons other than myself, except where due acknowledgement has been made. The
thesis has been completed during the course of enrolment in a PhD degree at the
University of Western Australia and has not been used previously for a degree or
diploma at any other institution.
__________________________________________________
Christopher Szota
November 2009
1
General Introduction
Introduction
The jarrah (Eucalyptus marginata Donn ex Sm.) forest is endemic to the Darling
Plateau of south-western Australia, and occurs on deep, lateritic soil profiles created
through in situ weathering of mainly granitic parent material (Churchward and
Dimmock 1989). The lateritic soils of the Darling Plateau are rich in aluminium
hydroxide minerals (McArthur 1991), which are mined as bauxite from the top 2-8
metres of the soil profile (Koch 2007).
Since 1989, the aim of bauxite mine restoration has been to re-establish a fully-
functioning jarrah forest which will re-develop the pre-mining values of the forest
(Koch 2007). Techniques currently used in bauxite-mine restoration such as direct-
return of topsoil, broadcast seeding, fertiliser application and deep-ripping of subsoil are
largely successful at rapidly establishing vegetation across the landscape (Grant et al.
1996; Koch et al. 1996; Ward et al. 1996; Koch 2007). Despite significant restoration
of the soil profile in all pits, some areas show poor growth of the two major tree species,
jarrah and marri (Corymbia calophylla Lindl.), several years after their successful
establishment. Factors limiting growth at this age can include impenetrable subsoils
(Enright and Lamont 1992; Passioura 2002; Mengler et al. 2006; Kew et al. 2007; Szota
et al. 2007). Such sites will often have higher rates of tree mortality; however, their
most striking attribute is that the surviving trees are significantly smaller.
The aim of this thesis is to determine whether soil constraints are responsible for
poor tree growth at low-quality restored bauxite mines. This thesis examines how the
below-ground root morphology and above-ground leaf-scale physiology of jarrah
respond to soil constraints at two contrasting (low-quality and high-quality) restored
bauxite-mine sites in south-western Australia. Furthermore, the development of jarrah
(using tree ring analysis) at these sites is examined in order to describe how soil
constraints influenced growth patterns over time. Overall, this multi-faceted approach
assesses the long-term capacity of jarrah to survive at restored bauxite mine sites.
2
The jarrah forest region
This section provides a brief summary of the study region, the northern jarrah forest.
Included here are specific aspects of the region which have a bearing on the present
study, rather than an exhaustive description (reviewed by Dell et al. (1989)).
The present study is located within the ‘northern jarrah forest’, a region which
has traditionally contained high-quality forest stands and where the bulk of bauxite
mining operations in the jarrah forest are located. The northern jarrah forest is confined
to the highly weathered lateritic soils of the Darling Range, Western Australia, located
between 13°51’ to 33°30’ and 115°50’ to 116°50’ (Bell and Heddle 1989). The eastern
boundary of the forest is represented by the 600 mm isohyet and the western boundary
by the Darling Scarp (Dell and Havel 1989). Prior to European settlement, the jarrah
forest covered ~5.3 x 106 ha; agricultural clearing has reduced this to ~3.3 x 106 ha, with
the majority situated on Crown land (Dell and Havel 1989).
The climate of the region is classified as Mediterranean, with hot, dry summers
and cool, wet winters. With respect to the jarrah forest as a whole, rainfall declines
dramatically from west (~1300 mm yr-1) to east (~600 mm yr-1), primarily due to
increasing distance from the coast. The present study took place near the town of
Dwellingup (32º43´S, 116º04´E), Western Australia. Located at the western edge of the
forest, Dwellingup has an annual rainfall of 1258 mm (Fig. 1). Approximately 90% of
annual rainfall occurs between April and October in Dwellingup, leaving only ~130 mm
falling over the hottest 5 months of the year; exposing the vegetation to a distinct, long
summer drought. Average daily maximum temperatures in the hottest two months of
the year (January and February) are 29.6 and 29.4°C and average daily minimum
temperatures are 14.2 and 14.4°C. On average, January as the hottest month of the year
records 16.1 days >30°C, 5 days >35°C and 0.3 days >40°C. During the coldest months
(June and July), average daily maximum temperatures are 15.8 and 14.9°C and average
daily minimum temperatures are 6.5 and 5.5°C. As the coldest month of the year, July
averages 1.8 days with minimum temperatures below 0°C.
This following section briefly describes the features of soil types specific to
areas of active bauxite mining in the northern jarrah forest, as opposed to exhaustively
describing the geology and soil types of the region. Gilkes et al. (1973), Sadlier and
Gilkes (1976) and Churchward and Dimmock (1989) describe the geology, landforms
and formation and distribution of soil profiles found throughout the jarrah forest.
3
The bulk of the jarrah forest is situated on the Darling Plateau which has
developed on the predominantly granitic crystalline rocks of the Yilgarn Block
(Churchward and Dimmock 1989). Deep, lateritic soil profiles form on all bedrock
materials of the plateau (Churchward and Dimmock 1989; McArthur 1991). Soil
profiles containing bauxite ore have 10 cm of nutrient-impoverished, organic-matter-
0
50
100
150
200
250
300
J F M A M J J A S O N DMonth
Rai
nfal
l (m
m)
05101520253035
Tem
pera
ture
(ºC
)
Figure 1. Long-term (72-year) average monthly maximum (white circles) and minimum (white squares) temperature and average monthly rainfall (black bars) for the town of Dwellingup (32º43´S, 116º04´E). Data recorded and supplied by the Australian Bureau of Meteorology at the Dwellingup weather station (009538), Western Australia, Australia.
stained, yellowish-brown sand over 0.5-1 m of yellowish-brown sand with a high
content (up to 75% w/w) of ferruginous ‘ironstone’ gravel (Churchward and Dimmock
1989). These surface layers are weathered from, and sit above, a ferruginous ‘lateritic’
duricrust (often referred to as ‘caprock’), which is 1-2 m thick, dense and frequently re-
cemented (Churchward and Dimmock 1989). The duricrust is high in sesquioxides of
iron and aluminium, primarily gibbsite and kaolinite (Gilkes et al. 1973), and gives way
to a mottled zone 4-6 m thick; also rich in iron and aluminium (Sadlier and Gilkes 1976;
Churchward and Dimmock 1989). Both the lateritic duricrust and the mottled zone are
mined as the ‘bauxite’ deposit, typically 5-8 m deep in total. Beneath the deposit, the
mottled zone gives way to a pallid or plasmic zone of highly-weathered (in situ)
kaolinitic clay before giving way to saprolite, saprock and finally bedrock (granite)
(Churchward and Dimmock 1989).
The northern jarrah forest is a ‘dry sclerophyll’, ‘open forest’ dominated by
sclerophyllous trees and shrubs (Dell and Havel 1989). The morphology of the ~784
plant species in the forest is typified by small, glabrous, sclerophyllous, alternately-
arranged leaves with reticulate venation and revolute leaf margins; all adaptations for
4
maximising energy capture under optimum conditions, protecting the photosynthetic
apparatus from excessive irradiance and minimising moisture loss during the long, dry
summer (Bell and Heddle 1989). A range of small trees (4-7 m), shrubs and ground-
covers exist on the forest floor, including Allocasuarina, Banksia, Persoonia,
Xanthorrhoea, Kingia and Macrozamia spp; however, the present study focussed on
jarrah (Eucalyptus marginata) and marri (Corymbia calophylla), the two dominant tree
species of the northern jarrah forest.
At high-quality sites in the high-rainfall (1200–1400 mm yr-1) south-west region
of the continent, jarrah exists as a tall tree (30-40 m) with a straight bole of 15-18 m and
DBH of up to 2 m (Dell and Havel 1989). On the margins of its distribution, in low
rainfall (~600 mm yr-1) northern and eastern regions, jarrah is found as a small, multi-
stemmed tree (Brooker and Kleinig 2001). Marri also occurs as a tall tree throughout
the jarrah forest and, similar to jarrah, is found as a mallee at the dry northern extreme
of its distribution (Brooker and Kleinig 2001). Marri is typically found in areas where
root development is limited and access to soil moisture is highly variable, for example,
in areas with shallow soil and in riparian zones susceptible to waterlogging (Harris
1956; Florence 1996). As rainfall and soil fertility increase to the south, karri
(Eucalyptus diversicolor F. Muell.) replaces jarrah as the dominant forest tree, while
marri remains a significant feature of the forest (Harris 1956). Eucalyptus wandoo
Blakely replaces jarrah as the dominant vegetation on its low-rainfall eastern margin,
and tuart (E. gomphocephala DC.) replaces jarrah on the coastal sands of the Swan
Coastal Plain to the west (Harris 1956).
Bauxite mining in the jarrah forest
This section provides a brief account of bauxite mining in the jarrah forest, describing
the process of bauxite extraction and the process of mine-site restoration. The term
‘restoration’ is used throughout, as per the terminology used by Aronson et al. (1993).
‘Restoration’ aims to return or restore the pre-disturbance structure, functioning,
diversity and dynamics to a site (Aronson et al. 1993). This includes re-establishing the
pre-disturbance flora, fauna, flows, cycles and processes (Hobbs and Norton 1996;
Whisenant 1999; Hobbs and Cramer 2003) of the ecosystem. In contrast, the aim of
‘rehabilitation’ is to repair damaged ecosystem functions to increase ecosystem
productivity (Aronson et al. 1993), that is, not necessarily to re-create the pre-
disturbance ecosystem.
5
In Western Australia, bauxite mining began in 1962 at Jarrahdale (32°20’S
116°3’E), approximately 50 kms south east of Perth. Bauxite mining is a major landuse
of the jarrah forest, with >550 ha yr-1 of forest mined by the major operator, Alcoa
World Alumina Australia (Koch 2007). The following section summarises current
mining and restoration practices used by Alcoa World Alumina Australia, described
recently by Koch (2007).
In general, bauxite mining in the jarrah forest is carried out as a shallow, open-
cut style of mining, where sand (referred to as ‘topsoil’) and gravel (referred to as
‘overburden’) layers above the bauxite deposit are stripped, the bauxite blasted and
removed, the pit is contoured into the surrounding landscape and a new soil profile
reconstructed on the mine pit floor. Bauxite mine pits range from 1-20 ha in size and
are typically mined to a depth of 5-8 m. Areas of forest which have been mined
visually represent a mosaic of mine pits inter-dispersed with islands of native
vegetation, where the extraction of bauxite was either not economically viable, or where
mining was disallowed due to social or environmental concerns.
Prior to mining, economic forest products ranging from high-grade sawlogs to
charcoal and mulch are salvaged from each area, and the remaining residue is
windrowed and burned. Topsoil (0-15 cm) is stripped and where possible returned to a
nearby area undergoing restoration (referred to as ‘direct-return’). The gravelly layer
beneath the topsoil and above the lateritic duricrust is removed and stockpiled until the
pit is restored. The lateritic duricrust is subsequently broken up via explosives or by
deep-ripping with a bulldozer. The duricrust and underlying bauxite ore deposit are
removed from the pit and hauled to a mobile crushing facility for processing. The
crusher feeds onto a conveyor belt which transports the ore to the refinery. At this
point, the pit is 2-10 m deep with vertical sides and a compacted clay (kaolinitic) floor
(Fig. 2).
Bauxite mine restoration techniques have developed over time as new
knowledge is acquired. The following description details current practice which differs
from the method used at the sites studied in this thesis (restoration methods used at
study sites are described in Chapter 1).
The first stage in mine pit restoration is to smooth down the vertical faces on the
pit to create a more natural contour, while ensuring that water does not flow from
restored areas into patches of remnant forest. Pits are then deep-ripped to 1.5 m using a
winged tine mounted on the back of a bulldozer. Riplines are spaced 1.6 m apart to
6
decrease soil compaction, facilitate root growth and increase infiltration of rainfall
(Croton and Watson 1987; Croton and Ainsworth 2007)
Stockpiled gravel is spread over the ripped mine floor to a depth of
approximately 0.5 m, followed by a 15 cm layer of topsoil obtained from a nearby area
being prepared for mining. The area is then contour-ripped to 0.8 m by a bulldozer with
three single tines which decreases compaction caused by soil return operations and
creates crests and furrows which encourage rainfall infiltration and prevent erosion.
Habitat logs and large rocks are distributed around restored pits to encourage re-
introduction of fauna to restored forest.
Figure 2. A typical bauxite mine pit post-mining and pre-restoration with remnants of the orange bauxite deposit on the pit ‘wall’ (with large ironstone boulders part of the remnant lateritic duricrust at the surface) and white kaolinitic clay visible on the ‘floor’ of the pit. Photograph by H. Lambers.
7
In 1966, rehabilitation and re-establishment aimed to install a fast-growing
timber resource with a higher resistance to the dieback fungus, Phytophthora
cinnamomi Rands (Tacey 1979a). A number of eucalypts from western and eastern
Australia were initially trialled for their suitability (Shea et al. 1975). In 1989, there
was a movement to restore the jarrah forest for conservation post-mining; which lead to
the expansion in research towards methods of increasing both flora and fauna species
diversity.
Current practice is to collect local seed of overstory and understory species
which is then broadcast across the site by the contour-ripping bulldozer during the drier
months of summer and autumn. Recalcitrant species are raised in a nursery and planted
out in winter. A once-off application of nitrogen, phosphorus and potassium fertiliser
with trace elements is broadcast by air in late winter.
Restored pits are assessed nine months after establishment to determine whether
stocking is adequate, and species diversity is assessed 15 months post-establishment.
Permanent plots are also established to assess species diversity at 6, 15, 20, 30 and 50
years of age.
Some restored areas show poor growth of the two major tree species, jarrah and
marri, several years after their successful establishment. The most likely explanation of
poor growth at this age is that soil compaction, as a result of the mining process,
restricts root development. In the Mediterranean climate of south-western Australia,
restriction of root systems to upper soil layers is likely to decrease the amount of
available water, resulting in increased water stress during seasonal drought. The
success of trees at restored sites will therefore depend on how their root morphology
responds to soil constraints, and how their physiological functioning responds to water
deficits during seasonal drought. The combination of these responses will ultimately
determine how their development over time is affected.
Morphological, physiological and developmental responses to drought
This section discusses how root-system morphology, tree physiology and growth
patterns respond to soil constraints and associated water deficits.
Root morphology and drought
Plants develop root systems in response to their growing environment, making the
complexity of their root system morphology a function of, in particular, water and
8
nutrient availability (Lynch 1995). The presence of physical, biological and/or
chemical soil constraints will increase the complexity of root systems, as plants will
need to increase root development in order to capture sufficient resources (Stone and
Kalisz 1991). Where soils are naturally deficient in nutrients and low in water
availability, such as the majority of the Australian continent, root systems increase in
complexity as they must scavenge for sparingly available nutrients and water; two key
resources which are often not accessible in the same place at the same time (Pate and
Dixon 1996).
Pate et al. (1998) excavated root systems of Banksia prionotes Lindl. growing in
the nutrient-impoverished (particularly phosphorus) sandy coastal plain of south-
western Australia. They described the root system as ‘dimorphic’; where the root
system could be described in two discrete functional units; a ‘lateral’ system comprised
of several horizontal roots bearing highly specialised ‘cluster’ or ‘proteoid’ roots which
scavenge for nutrients in surface soil layers; and a vertical system consisting of a single,
unbranched ‘taproot’ which descends vertically directly beneath the stem to search for
water at depth (Pate et al. 1998). Shoot growth in early summer, when water becomes
limiting, is dependent on nutrients acquired by the lateral system during the previous
wet season; while water is supplied by the taproot (Pate et al. 1998; Zencich et al. 2002;
Veneklaas and Poot 2003). Furthermore, a number of studies have now confirmed the
theory of ‘hydraulic lift’, where water is re-distributed between roots in order to prevent
their desiccation (Burgess et al. 1998; Pate and Dawson 1999; Burgess et al. 2000), thus
in the situation of B. prionotes, water accessed at depth during summer can be
redistributed to lateral roots to prevent their desiccation (Pate et al. 1998).
Wildy and Pate (2002) excavated root systems of the mallee, E. kochii Maiden
& Blakely subsp. plenissima Gardner (Brooker), growing in the low-rainfall (319 mm
yr-1) wheatbelt of Western Australia. In response to extremely low water availability,
these trees developed a number of deeply-penetrating vertical roots directly below the
stem; as well as a number which descended from shallow lateral roots (Wildy and Pate
2002). More than 40% of below-ground biomass of these trees was allocated to vertical
roots (Wildy and Pate 2002), emphasising the strong dependence on water at depth in
this low-rainfall environment. Production of a large number of vertical roots indicates a
response to soil limitations. Unlike B. prionotes growing on deep coastal sands which
develops a single, large vertical root (Pate et al. 1998), E. kochii often encounters clay
9
hardpans which restrict root growth (Wildy et al. 2004a); therefore necessitating the
development of multiple vertical roots in order to secure water at depth.
In an even more extreme environment (rainfall <300 mm yr-1, evaporation
>4000 mm yr-1, average summer temperature >40°C), Grigg et al. (2008) studied root
systems in the Great Sandy Desert of central Western Australia in order to explain the
distribution of tree and shrub species. The largest tree species (basal stem diameter up
to 40 cm), Corymbia chippendalei D.J. Carr & S.G.M.Carr, was restricted to the top of
large sand dunes, where roots did not emerge from the root crown until 1-2 m below the
surface, at which point many large (30-100 mm diameter) roots emerged and descended
diagonally to search for stored water deep below the surface. The root systems of this
species is well adapted to this growing environment; the lack of nutrient-seeking lateral
or surface roots is a function of the nutrient-impoverished topsoil (Grigg et al. 2008),
furthermore not producing roots in dry 1-2 m of the soil profile decreases its chance of
desiccation.
Poot and Lambers (2003) compared highly-specialised root systems of rare
Hakea species growing on shallow ironstone rock in south-western Australia with more
widely distributed commonly-occurring Hakea species. Shallow-soil species were
highly adapted to their growing environment by maintaining high initial root mass ratios
and investing more biomass in multiple, long, lateral roots such that they could rapidly
explore a large surface area, presumably in order to encounter cracks and fissures in the
rock (Poot and Lambers 2003; 2008). Widely distributed species invested more in short
laterals and cluster roots at the base of the plant, signifying their lack of need to
scavenge for water at depth and instead focus on rapid access to nutrients (Poot and
Lambers 2008). This study is an excellent example of highly-specialised root system
morphologies and patterns of root development forcing a trade-off between acquisition
of water and nutrients (Futuyma and Moreno 1988).
Kimber (1974) first described the unique root system that jarrah produces in
response to granite-derived lateritic soil profiles found throughout the Northern jarrah
forest. In the unmined forest, jarrah trees produce a dense lateral root network which
occupies the gravel-dominated soil layer above the lateritic duricrust (Kimber 1974).
Lateral roots are able to extend up to 20 m from the base of the tree (Abbott et al. 1989).
Two specialised vertical root system structures branch from lateral roots: ‘riser’ roots
which grow upwards towards the soil surface and scavenge for nutrients; and ‘sinker’
roots which descend vertically to seek out water at depth (Kimber 1974; Abbott et al.
10
1989). Cracks and fissures in the lateritic duricrust allow penetration of sinker roots
into the bauxite layer below (Abbott et al. 1989). Beneath the friable bauxite layer,
sinker roots gain access to moisture-bearing kaolinitic clay through ancient root
channels created by previous vegetation structures (Dell et al. 1983). Dell et al. (1983)
suggested that each tree can gain access to 100–200 ancient root channels which can
extend up to 40 m below the surface.
The bulk of the root length in the jarrah forest is found in the coarse-textured
sandy surface soil which has the greatest potential to supply water to trees in winter
(Carbon et al. 1980). Indeed, jarrah has been shown to draw water from the top of the
soil profile when topsoil moisture is highest in winter and early spring (Farrington et al.
1996). As the surface layers dry out during the dry season, trees draw water from
deeper in the soil profile via vertical sinker roots (Farrington et al. 1996).
Mining-related compaction (creation of impenetrable layers and/or increasing
bulk density) is an obvious threat to root development, in particular, the development of
roots which seek out moisture at depth. Enright and Lamont (1992) found that mining-
related compaction prevented vertical roots from accessing water at depth and resulted
in high mortality of Banksia species at restored mineral sand mines in south-western
Australia. Rokich et al. (2001) showed that taproots of Banksia species produced a high
number of laterals after the taproot was unable to penetrate the subsoil of rehabilitated
soil profiles; markedly different to its root morphology in unmined soil profiles where
the taproot remains vertical and does not branch. Banksia species at restored sites also
failed to produce a dominant taproot, a key specialisation of these species for surviving
drought, instead producing a number of smaller roots (Rokich et al. 2001).
At restored bauxite mine sites, soil profiles are heterogeneous and contain a
range of regolithic materials that, due to their nature (Kew et al. 2007) as well as the
influence of mining (Croton and Watson 1987), can prevent tree root penetration
(Mengler et al. 2006). Compaction of the kaolinitic material on the floor of mined area
is relieved through deep-ripping (Croton and Watson 1987). Deep-ripping has been
shown to increase survival and growth for a range of tree species on a number of
different soil types in a number of contrasting environments (Varelides and Kritikos
1995; Ashby 1997; Nadeau and Pluth 1997; Lacey et al. 2001).
Previous studies on rehabilitated bauxite mines in south-western Australia have
found that the root systems of young trees were restricted to friable soil in riplines (Shea
et al. 1975; Tacey 1979b; Dell et al. 1983; Kew et al. 2007) on granite-derived lateritic
11
soils. In certain material, roots can be confined to riplines following deep-ripping
operations as a result of poor soil loosening and localized compaction caused by the
ripping tine (Spoor and Godwin 1978; Kew et al. 2007). To increase their chance of
long-term survival, trees at restored sites will need to penetrate below the ripping depth
and gain access to water-holding kaolinitic clay in the pallid zone (Dell et al. 1983;
Farrington et al. 1996).
This thesis (Chapter One) examines the root morphology of jarrah in relation to
deep-ripping at two restored bauxite mine sites with different reconstructed soil profiles.
Chapter One aims to determine whether jarrah trees retain the ability to develop highly-
specialised root systems and thereby gain sufficient access to water at depth at restored
sites. Given the importance of deep-ripping in rehabilitation of the soil profile, this
investigation will determine how deep-ripping operations affect root system
morphology, and in particular, whether trees change the allocation of biomass to
different root-types depending on their immediate soil conditions.
Physiological mechanisms and drought
Plants exposed to seasonal drought have developed a range of physiological
mechanisms that enhance their survival. Species have been classified according to their
response to drought via the terms ‘drought-avoiding’ and ‘drought-tolerating’ (Levitt
1972). Drought-avoiding species have mechanisms which avoid water deficits during
drought, including morphological mechanisms such as a deep root system which can
access soil moisture; and physiological mechanisms such as stomatal closure. Drought-
tolerating species must endure exposure to drought; however, they possess
physiological mechanisms which allow them to maintain turgor despite losing water
status, thereby allowing continued physiological functioning during drought.
Studies of drought-response mechanisms in eucalypts have revealed wide
variation with regard to the type of mechanism and the magnitude by which it
contributes to survival during drought (Pook et al. 1966). Eucalypts can show both
drought-avoiding and drought-tolerating responses to drought (Davidson and Reid
1989). The most common drought-response mechanisms in eucalypts are stomatal
closure (drought-avoidance) and ‘osmotic adjustment’ (drought-tolerance).
Stomatal closure is the principal mechanism by which plants reduce water loss
from the leaf to the atmosphere (Kramer and Boyer 1995). Under well-watered, non-
limiting conditions, stomatal aperture is maximised and plants take up carbon dioxide
12
and as a result, release water (Lambers et al. 1998). When water becomes limiting,
guard cell turgor declines, resulting in a reduction in stomatal aperture; a reaction which
results in minimisation of water loss from the leaf (Kramer and Boyer 1995). The water
status of plants is closely related to stomatal aperture; and any substantial decrease in
plant water status can result in stomatal closure. Stomatal closure has also been shown
to occur in response to climatic factors, specifically, increasing VPD over the day at the
onset of seasonal drought (Prior et al. 1997; Thomas and Eamus 1999). Hormonal
regulation of stomatal aperture has been demonstrated, where roots ‘detect’ declining
soil moisture and release abscisic acid (ABA) into the xylem, resulting in stomatal
closure (Davies et al. 1990; Davies and Zhang 1991; Tardieu and Davies 1992). It has
been commented; however, that a signal release from far downstream would not reach
the leaf in time prevent desiccation, particularly in tall trees (Kramer 1988).
Eucalypts differ substantially in the sensitivity of their stomates to internal and
external water deficits. In general, eucalypts from high-rainfall zones and/or with
higher water availability have a higher stomatal sensitivity than those from low-rainfall
zones. Such species typically lose turgor at higher water status. E. pauciflora Sieb. ex
Spreng. from the Snowy Mountains of New South Wales loses turgor between -1.25 and
-2.12 MPa (Körner and Cochrane 1985), Eucalyptus grandis Hill ex Maiden from the
moist subtropics of southern Queensland loses turgor at approximately -1.4 MPa (Fan et
al. 1994), E. regnans F. Muell. from high-rainfall mountain ranges in Victoria loses
turgor at -1.9 MPa (Ashton and Sandiford 1988), a humid, coastal provenance (>1400
mm yr-1) of E. cloeziana F. Muell. from southern Queensland lost turgor at -1.97 MPa,
compared to -2.25 MPa for a dry, inland provenance (<700 mm yr-1) of the same species
(Ngugi et al. 2003). In contrast, low-rainfall eucalypts tend to maintain turgor at lower
water status, therefore the sensitivity of their stomata is low compared with high-rainfall
eucalypts. E. leucoxylon F. Muell. (a small to medium-sized tree from southern
Flinders Ranges, Mount Lofty Range, Kangaroo Island and the south-east of South
Australia (Brooker and Kleinig 1999)) and E. platypus subsp. platypus Hook. (a small
tree scattered along the coastal and subcoastal plains between Albany and Esperance,
Western Australia (Brooker and Kleinig 2001)) showed low stomatal sensitivity and lost
turgor at -3.9 MPa in response to drought at a low-rainfall (480 mm yr-1) site (White et
al. 2000). Eucalypts from xeric environments including E. polyanthemos Schauer
(Myers and Neales 1986; Merchant et al. 2007), E. behriana F. Muell. (Myers and
Neales 1986), E. microcarpa Maiden (Myers and Neales 1986). E. cladocalyx F. Muell.
13
and E. tricarpa L.A.S. Johnson & K. Hill (syn. E. sideroxylon subsp. tricarpa L.A.S.
Johnson) (Merchant et al. 2007) also demonstrate little stomatal regulation and lose
turgor between -1.9 and -3.6 MPa.
Eucalypts from low-rainfall environments are typically highly drought-tolerant
as they are able to maintain positive turgor and physiological functioning during
drought. The ability of plants to maintain turgor as water status (water potential)
declines is typically attributed to reduction of osmotic potential through ‘osmotic
adjustment’; via active accumulation of organic solutes in the cytoplasm, or by passive
concentration of solutes by reducing cellular water (Turner and Jones 1980; Turner
2006). Eucalypts have demonstrated either the active accumulation of solutes or elastic
adjustment in order to maintain positive turgor at low water status. Eucalypts with high
drought-tolerance maintain turgor by having an inherently low osmotic potential or
more elastic leaf tissue compared to those with low drought-tolerance. E. leucoxylon
showed a high bulk modulus of elasticity (23.6 and 25.8 MPa) and low osmotic
potential at the turgor loss point (-3.81 and -3.92 MPa) in both summer and winter at a
low-rainfall site (480 mm yr-1); therefore its underlying mechanism for drought-
tolerance was an inherently low osmotic potential (White et al. 2000). In contrast, bulk
elastic modulus of E. platypus decreased in response to drought at the same low-rainfall
site; therefore its underlying drought-tolerance mechanism was elastic adjustment
(White et al. 2000).
Jarrah is a species well-adapted to surviving extended periods of drought. The
highly-adapted root system of the species provides the major mechanism by which
mature trees maintain water status (avoid drought) during the dry summer months. This
water store is, however, many metres below the surface, therefore trees require
additional physiological mechanisms to survive drought in the years prior to roots
accessing soil moisture at depth (Prior and Eamus 1999).
On the forest floor, seedlings are subjected to significant water stress (<-1.5
MPa) during summer as a result of competition, primarily for soil moisture, from the
overstorey (Stoneman et al. 1995); one of the key reasons behind seedling mortality of
>90% in the first year (Harris 1956). Under such water limiting conditions, the primary
mechanism by which jarrah seedlings regulate water loss is through stomatal closure
(Stoneman et al. 1994; Crombie 1997). Stoneman et al. (1994) also found that
seedlings in the glasshouse osmotically adjusted once predawn leaf water potentials fell
below -1.5 MPa; however, this response has not been demonstrated by seedlings in the
14
field. In the field and the glasshouse, rates of leaf growth and photosynthesis in jarrah
seedlings decline sharply as plant water status declines (Stoneman et al. 1994;
Stoneman et al. 1995).
Physiological studies of jarrah have shown that mature trees suffer lower water
stress than seedlings, saplings and young trees (Crombie et al. 1988; Crombie 1992;
Stoneman et al. 1995; Crombie 1997), presumably a result of roots gaining access to
moisture at depth as trees mature. Prior to securing access to water resources deep in
the soil profile, jarrah saplings remain exposed to high levels of water stress, often
achieving predawn leaf water potentials below -2.5 MPa during drought (Crombie
1997). Jarrah saplings continue to rely on stomatal closure as their primary mechanism
for regulation of water loss during drought (Crombie 1997). The link between root
development and water status has been found to hold true for jarrah forest species,
where understorey vegetation with shallow root systems suffer greater water stress
during drought compared to deep-rooted overstorey species (Crombie et al. 1988;
Crombie 1992).
As a mature tree in the forest, jarrah can access water deep in the soil profile
(Farrington et al. 1996) through ancient root channels (Dell et al. 1983) which can
allow the maintenance of high rates of transpiration over summer (Grieve 1956;
Colquhoun et al. 1984). It was initially suggested that water use of mature jarrah is
‘unregulated’ once roots have access to soil moisture at depth (Grieve 1956). Doley
(1967) and Carbon et al. (1981a), however, showed that transpiration rates decreased
with increasing leaf water deficit, indicating stomatal regulation during periods of high
evaporative demand and low water availability. Crombie (1992) demonstrated stomatal
closure over the day in mature jarrah at both low-rainfall (750 mm yr-1) and high-
rainfall sites (1250 mm yr-1) during midsummer. He also showed lower average midday
stomatal conductance during drought (January – April) compared to periods with high
soil moisture (October – November). The need for mature trees to regulate water loss
through stomatal closure is clearly related to the availability of soil moisture and the
demand for water from the atmosphere.
It has been demonstrated that the physiology of larger, older trees is often
markedly different to that of smaller, younger trees (Crombie 1997; Kolb and Stone
2000; Niinemets 2002; Rust and Roloff 2002) and coppice (Crombie 1997; Wildy et al.
2004b). Therefore, knowledge gained from the study of mature jarrah and marri
physiology may not be directly applicable to younger stands. Furthermore, the
15
physiology of trees at restored bauxite-mine sites may differ from that of trees growing
on undisturbed soil profiles. It is therefore extremely important to increase the number
of studies on the physiological functioning and water relations of forest stands growing
on restored sites.
Seedlings at restored sites differ markedly with regard to resource availability
compared to those at unmined sites. In the absence of an overstorey, at both mined and
unmined sites, jarrah seedlings show lower water stress, faster growth and higher
photosynthetic rates compared to seedlings at unmined forest sites where the overstorey
was retained (Stoneman et al. 1995). Removal of competition from mature trees
increased light, soil moisture and soil temperature, all of which have a positive
influence on the growth of seedlings on the forest floor (Stoneman and Dell 1993;
Stoneman et al. 1994; Stoneman et al. 1995).
Early physiology and water relations studies at restored sites focussed on
comparing water use and water stress of non-local eucalypts (Tacey 1979a) to unmined
mature jarrah and marri. The eucalypts studied included marri, Eucalyptus wandoo, E.
maculata Hook., E. resinifera Sm., E. saligna Sm., E. microcorys F. Muell., E.
muelleriana Howitt and E. globulus Labill. (Carbon et al. 1981b; Colquhoun et al.
1984). Colquhoun et al. (1984) showed that midday water potentials of 3-9 year old
marri on restored sites were comparable to marri in adjacent unmined forest. Carbon et
al. (1981b) found the same result: 6-8 year-old E. microcorys and E. muelleriana at
restored sites suffered approximately the same level of water stress (leaf water potential)
as unmined mature jarrah and marri during the summer drought. In contrast with these
observations, these same authors also showed that transpiration was lower for the young
restored trees compared with the mature unmined trees. These findings suggest that
either the mature trees had access to a greater soil moisture store or that the young trees
may have maintained water status by stomatal closure rather than access to water at
depth. Interpretation of these results is complicated by the difference in developmental
stage and height between the young replanted trees at the restored sites and mature trees
at unmined sites.
Bleby (2003) undertook the first substantial investigation of physiology and
water relations at restored bauxite mine sites by comparing 6-9-year-old jarrah saplings
at a high-rainfall site (~1200 mm yr-1) with those at a low-rainfall site (~600 mm yr-1).
Bleby (2003) showed that jarrah saplings are anisohydric, with leaf water potential,
stomatal conductance and transpiration varying seasonally according to supply of water
16
from the soil and evaporative demand from the atmosphere. Saplings at the low- and
high-rainfall sites showed similar minimum water potentials (-2.5 and -2.7 MPa) during
the summer drought despite lower water availability at the low-rainfall site. Bleby
(2003) also showed, and Warren et al. (2007) confirmed, that stomatal closure was the
primary drought-tolerance mechanism at both sites and that osmotic adjustment did not
occur. Effective stomatal regulation may explain why minimum water potentials during
drought were similar at both sites despite obvious differences in available water. In a
summer irrigation experiment at both sites, Bleby (2003) showed that saplings in the
high-rainfall site increased stomatal conductance, while those at the low-rainfall site did
not. This result was explained by the premise that saplings at the low-rainfall site had a
less conductive water transport system, such that transpiration and stomatal conductance
were low, even when water supply was not limiting (Bleby 2003). Seasonal data
showed that saplings at the low-rainfall site were able to achieve similar ‘maximum’ gs
in spring/early summer as those at the high-rainfall site (Bleby 2003); therefore an
alternative interpretation of these data is that gs was being limited by something other
than water availability at the low-rainfall site, such as high vapour pressure deficit
(Macfarlane et al. 2004); or by an internal mechanism such as release of abscisic acid
(ABA) from the roots (Davies et al. 1990; Davies and Zhang 1991; Tardieu and Davies
1992).
Water relations and physiological response to drought are yet to be measured in
mature stands of restored jarrah forest, primarily because the oldest sites are only 20
years old. Until these stands reach maturity, the problem remains of finding unmined
stands at the same stage of development as restored stands to use as a valid comparison
remains.
Despite being a co-dominant species in jarrah forest stands, studies of marri
(Corymbia calophylla), and in particular, physiological studies of marri have been
limited (Colquhoun et al. 1984; Crombie et al. 1988; Crombie 1992). In studies where
marri has been included, it is typically discussed in less detail than jarrah, presumably
because it represents less of the stand (typically 20-40%) and has historically had less
economic value. Previous studies have also grouped jarrah and marri together to
represent the overstorey and have not had the specific aim of searching for inherent
differences between the two species (Crombie 1992). Studies of co-occurring eucalypts
indicate that they often possess different physiological mechanisms and/or access
different resource pools (Pook et al. 1966; Burdon and Pryor 1975; Davidson and Reid
17
1989; Eberbach and Burrows 2006; Grigg et al. 2008). It is extremely important to
understand what inherent differences exist between the two species such that
performance post-major disturbance (such as bauxite mining) can be predicted and
managed appropriately.
There is significant evidence from previous studies in the jarrah forest that jarrah
and marri differ in the magnitude to which they suffer water stress. Crombie (1992)
showed in a mature jarrah forest stand that marri maintained midday leaf water
potentials 22-34% higher than jarrah at a high-rainfall site (1250 mm yr-1); and 24-47%
higher than jarrah at a low-rainfall site (750 mm yr-1) during the dry summer months
(January – March). The same trend was reflected in predawn leaf water potentials at the
same sites (Crombie et al. 1988). Carbon et al. (1981a) compared water relations of
jarrah with marri, yarri (Eucalyptus patens Benth.) and flooded-gum (Eucalyptus rudis
Endl.) at a range of mature jarrah forest stands and showed that jarrah maintained more
negative water potentials than marri, yarri and flooded-gum in late summer. Colquhoun
et al. (1984) showed that marri maintained higher midday water potentials (-1.8 MPa)
than jarrah (-2.4 MPa) during summer. The mechanism by which mature marri is able
to maintain higher water status during drought is unknown.
No studies have thus far compared the physiological response to drought of
jarrah and marri saplings at restored sites, despite significant evidence suggesting an
inherent difference between mature trees of the two species (Carbon et al. 1981a;
Colquhoun et al. 1984; Crombie et al. 1988; Crombie 1992). In the unmined forest,
marri tends to colonise areas where root development is limited and access to soil
moisture is highly variable, such as in areas with shallow soil and riparian zones
susceptible to waterlogging (Harris 1956; Florence 1996). If marri has a greater
capacity to survive sites with high variation in water availability, then it has a high
potential to be deployed at sites where soil profile restoration has been sub-optimal.
Early studies at restored sites have shown that although marri shows lower resistance to
water loss, it maintains a higher water status than a range of other eucalypts including E.
wandoo, E. maculata, E. resinifera and E. saligna (Colquhoun et al. 1984).
Furthermore, at hostile restored sites, such as sites where deep-ripping has been
ineffective, marri shows higher survival and performance compared with jarrah (J. Koch
pers. comm.). These results and observations have lead to the inclusion of marri as well
as jarrah in describing patterns of water stress in relation to restored site quality in the
present study.
18
Chapter Two aims to describe the response of jarrah to seasonal drought, in
order to describe the nature and magnitude of stresses experienced at low- and high-
quality restored bauxite mine sites. The ability of jarrah to maintain water status and
physiological functioning during drought will be assessed and compared to marri, to
determine whether any inherent differences in the drought-response mechanisms of the
two species exist.
Growth and development in response to drought
Plants from dry environments tend to invest more resources below-ground than above-
ground, particularly early in their development (Lambers and Poorter 1992). This
adaptation increases the ability of plants to explore a greater soil volume for moisture,
while at the same time, minimising the leaf area from which to lose water. Jarrah is one
such species which spends many years on the forest floor developing below-ground
resources (root system and lignotuber) prior to stimulating vigorous crown growth. The
necessity for this pattern of temporal development is driven by two major factors:
competition from mature trees, heterogeneous soil profile and the long summer drought.
In the un-disturbed forest, jarrah seedlings grow 2-10 cm in the first year (Abbott et al.
1989) and can remain this size for 6-10 years (Abbott and Loneragan 1984). During
this time they develop a lignotuber and begin developing a root system. Stems are often
damaged by fire or herbivores, resulting in multiple shoots emerging from the
lignotuber (Abbott et al. 1989). These shoots can remain <1.5 m for 15-20 years until
the lignotuber is ~10 cm in diameter (Harris 1956) and below-ground resources are
sufficient to sustain increased shoot growth in the form of a dominant shoot. This shoot
then develops into a sapling and eventually a mature tree (Abbott and Loneragan 1984;
Abbott et al. 1989).
The growth of jarrah trees at disturbed sites, such as heavily logged or mined
sites, is rapid and bypasses several of the initial developmental stages (Abbott et al.
1989). Seedlings planted at rehabilitated patches of heavily-logged unmined forest
rapidly developed above-ground resources, achieving apical dominance within 2 years
(Harris 1956), as opposed to 15-20 years in undisturbed forest (Abbott and Loneragan
1984; Abbott et al. 1989). At restored bauxite mine sites, initial growth rates of
seedlings are significantly faster than at unmined forest stands (Stoneman et al. 1995).
Jarrah at restored mine sites can grow >3 m tall in the first 4-5 years (Ward and Koch
1995) and achieve 9 m in 13 years (Koch and Ward 2005); with 1 m yr-1 considered to
19
be the average for young restored sites (Koch and Samsa 2007). Similar growth rates
can be achieved by jarrah saplings regenerating from seed at high-quality cut-over
unmined forest which achieve 0.9 m yr-1 (at age 5), 0.5 m yr-1 (at age 20) and 0.3 m yr-1
(at age 40) (Stoate and Wallace 1938; Harris 1956). Enhanced growth of seedlings at
restored sites is primarily the result of removal of competition from mature trees which
increases light, soil moisture and soil temperature, all of which have a positive influence
on the growth of seedlings (Stoneman and Dell 1993; Stoneman et al. 1994; Stoneman
et al. 1995).
Rapid initial growth bypasses the lignotuberous seedling and ground coppice
stage. Plants instead develop rapidly into saplings (Abbott and Loneragan 1984). Given
that seedlings at unmined forest stands spend their first years developing below-ground
resources rather than those above-ground (Abbott and Loneragan 1984; Abbott et al.
1989); it is likely that the rapid above-ground development of seedlings at restored sites
is not accompanied by a comparative investment in below-ground resources (Shea et al.
1975). Since root development is difficult to quantify in the field, particularly over
time, rates of above-ground development are often used as a proxy for below-ground
development (Koch and Samsa 2007). Moreover, Shea et al. (1975) and later Dell et al.
(1983) showed that above-ground growth was much higher than below-ground growth
for a range of eucalypts (from eastern Australia) planted at restored bauxite mines.
High above-ground biomass relative to below-ground biomass in an environment
characterised by long periods of drought exposes trees to a higher risk of desiccation
(Markesteijn and Poorter 2009). It is unknown as to whether above-ground growth of
jarrah at restored sites is restricted when root system development is constrained.
Primary roots of eucalypts, particularly the vertical taproot, develop rapidly in the first
year of growth (Jacobs 1955; Florence 1996), therefore, in the presence of soil
constraints such as inherently shallow soil or compacted soil, vertical root growth is
more than likely affected in the first years of growth (Stone and Kalisz 1991). An
analysis of above-ground growth over time, as carried out in this thesis, taking into
account soil characteristics and root system morphology, allows an assessment of the
relationship between above- and below-ground development of jarrah at restored
bauxite mine sites.
Chapter Three aims to reconstruct the above-ground growth history of jarrah at
restored bauxite mine sites in order to determine whether soil constraints have restricted
above-ground development at an early age. Chapter 3 will describe above-ground
20
growth patterns over time in relation to below-ground morphology at two restored
bauxite mine sites with contrasting soil profiles. The nature of this relationship will
provide evidence as to whether patterns of temporal development of jarrah are as
conducive to long-term survival at restored sites as they are on unmined sites.
Annual growth data since establishment are typically unavailable at restored
sites; therefore this study will apply the technique of tree-ring analysis to describe
patterns of diameter increase over time. Tree-ring analysis relies on annual events
which slow or stop cambial activity to the point where a distinct ring is evident (Fritts
1976). The strongly seasonal growth phenology of jarrah produces tree-rings that are
suited for analysis for the purpose of describing patterns in growth. Stem diameter
growth occurs from mid-autumn to early summer (Abbott et al. 1989), prior to any
vigorous crown growth (Harris 1956). Growth of dense wood with few pores is
stimulated by break-of-season rainfall in autumn, which then gradually changes to light
wood with many pores as growth rates increase during spring, until terminating when
water becomes limiting in summer (Abbott et al. 1989). Tree-ring analysis has
previously been successfully applied to mature jarrah trees (~40-400 years old) for a
range of purposes (Nicholls 1974; Burrows et al. 1995; Whitford 2002; Schulze et al.
2006).
Thesis Outline
Chapter One
Chapter One aims to determine whether jarrah saplings at restored bauxite mine sites
can produce root system morphologies similar to those produced by trees at unmined
sites. Soil profiles and root system morphologies of jarrah saplings are described in
relation to deep-ripping and site quality at two restored bauxite mine sites (low- and
high-quality). Allocation to different root system structures in response to whether the
tree was situated on a crest or ripline (created by deep-ripping operations) is quantified
at the two sites, to interpret the response of jarrah saplings to soil constraints and to
determine the effectiveness of deep-ripping operations in facilitating root growth into
the subsoil.
Chapter Two
Chapter Two explores differences in physiological response to drought in relation to site
quality, of the two major tree species at restored sites, jarrah and marri. Water status
21
(water potential, osmotic potential and relative water content) and physiological
functioning (stomatal conductance and photosynthesis) are measured on a monthly basis
over 18 months (two drought cycles) in order to describe the nature and magnitude of
drought stress that trees at restored sites are exposed to. The physiological response to
drought of marri is compared with jarrah to determine whether any inherent differences
exist between these co-occurring eucalypts, a result that would influence species
selection at restored sites.
Chapter Three
Chapter Three takes the unique approach of using tree-ring analysis to determine how
soil constraints influence the above-ground development of jarrah saplings over time.
Annual growth rings are identified and annual diameter growth increments quantified
such as to describe patterns of above-ground growth over time. Given the observed
effect of deep-ripping on root system morphology (Chapter 1), the distinction is made
between trees situated on crests and in riplines in analysing patterns of above-ground
growth. Relationships between annual above-ground growth and climatic variables
(rainfall, temperature and vapour pressure deficit) are also determined in relation to tree
situation and site quality. It is expected that trees at sites where root systems are
restricted to upper soil layers will have a higher dependence on rainfall compared with
trees at sites where root systems are able to access water at depth.
Concluding Discussion
The Concluding Discussion compiles the results from the three investigations on
analysing the drought-response mechanisms of jarrah at restored bauxite mine sites, and
discusses their relevance to bauxite mine restoration practices in the jarrah forest of
south-western Australia. Finally, the limitations of the thesis and recommendations for
areas of future research that will continue to improve jarrah forest restoration practices
are discussed.
References
Abbott I, Dell B and Loneragan O 1989 The jarrah plant. In The jarrah forest: a
complex Mediterranean ecosystem. Eds. B Dell, J J Havel and N Malajczuk. pp
41-51. Kluwer Academic Publishers, Dordrecht.
22
Abbott I and Loneragan O 1984 Growth rate and long-term population dynamics of
jarrah (Eucalyptus marginata Donn ex Sm.) regeneration in Western Australian
forest. Australian Journal of Botany 32, 353-362.
Aronson J, Floret C, LeFloc'h E, Ovalle C and Pontanier R 1993 Restoration and
rehabilitation of degraded ecosystems in aris and semi-arid lands. I. A view from
the south. Restoration Ecology 1, 8-17.
Ashby W C 1997 Soil ripping and herbicides enhance tree and shrub restoration on
stripmines. Restoration Ecology 5, 169-177.
Ashton D H and Sandiford E M 1988 Natural hybridisation between Eucalyptus
regnans F. Muell. and E. macroryncha F. Muell. in the cathedral range, Victoria.
Australian Journal of Botany 36, 1-22.
Bell D T and Heddle E M 1989 Floristic, morphologic and vegetational diversity. In
The jarrah forest : a complex Mediterranean ecosystem. Eds. B Dell, J J Havel
and N Malajczuk. pp 53-66. Kluwer Academic Publishers, Dordrecht.
Bleby T M 2003 Water use, ecophysiology and hydraulic architecture of Eucalyptus
marginata (jarrah) growing on mine rehabilitation sites in the jarrah forest of
south-western Australia. PhD Thesis, The University of Western Australia,
Perth.
Brooker M I H and Kleinig D A 1999 Field guid to eucalypts. Vol 1, South-eastern
Australia. Bloomings Books, Melbourne. pp. 353.
Brooker M I H and Kleinig D A 2001 Field guide to eucalypts. Vol. 2, South-western
and southern Australia. Bloomings Books, Melbourne. pp. 428.
Burdon J J and Pryor J D 1975 Interspecific competition between eucalypt seedlings.
Australian Journal of Botany 23, 225-229.
Burgess S S O, Adams M A, Turner N C and Ong C K 1998 The redistribution of soil
water by tree root systems. Oecologia 115, 306-311.
Burgess S S O, Pate J S, Adams M A and Dawson T E 2000 Seasonal water acquisition
and redistribution in the Australian woody phreatophyte, Banksia prionotes.
Annals of Botany 85, 215-224.
Burrows N D, Ward B and Robinson A D 1995 Jarrah forest fire history from stem
analysis and anthropological evidence. Australian Forestry 58, 7-16.
Carbon B A, Bartle G A and Murray A M 1981a Patterns of water stress and
transpiration in jarrah (Eucalyptus marginata Don ex Sm.) forests. Australian
Forest Research 11, 191-200.
23
Carbon B A, Bartle G A and Murray A M 1981b Water stress, transpiration and leaf
area index in eucalypt plantations in a bauxite mining area in south-west
Australia. Australian Journal of Ecology 6, 459-466.
Carbon B A, Bartle G A, Murray A M and Macpherson D K 1980 The distribution of
root length, and the limits to flow of soil water to roots in a dry sclerophyll
forest. Forest Science 26, 656-664.
Churchward H M and Dimmock G M 1989 The soils and landforms of the northern
jarrah forest. In The jarrah forest: a complex Mediterranean ecosystem. Eds. B
Dell, J J Havel and N Malajczuk. pp 13-21. Kluwer Academic Publishers,
Dordrecht.
Colquhoun I J, Ridge R W, Bell D T, Loneragan W A and Kuo J 1984 Comparative
studies in selected species of Eucalyptus used in rehabilitation of the northern
jarrah forest, Western Australia. I. Patterns of xylem pressure potential and
diffusive resistance of leaves. Australian Journal of Botany 32, 367-373.
Crombie D S 1992 Root depth, leaf area and daytime water relations of jarrah
(Eucalyptus marginata) forest overstorey and understorey during summer
drought. Australian Journal of Botany 40, 113-122.
Crombie D S 1997 Water relations of jarrah (Eucalyptus marginata) regeneration from
the seedling to the mature tree and of stump coppice. Forest Ecology and
Management 97, 293-303.
Crombie D S, Tippett J T and Hill T C 1988 Dawn water potential and root depth of
trees and understorey species in south-western Australia. Australian Journal of
Botany 36, 621-631.
Croton J T and Ainsworth G L 2007 Development of a winged tine to relieve mining-
related soil compaction after bauxite mining in Western Australia. Restoration
Ecology 15, (Supplement) S48-S53.
Croton J T and Watson G D 1987 Mining related compaction - a case study in the
Darling Range, Western Australia. pp 1-19. ALCOA World Alumina Australia,
Perth, W.A.
Davidson N J and Reid J B 1989 Response of eucalypt species to drought. Australian
Journal of Ecology 14, 139-156.
Davies W J, Mansfield T A and Hetherington A M 1990 Sensing of soil water status
and the regulation of plant growth and development. Plant, Cell and
Environment 13, 709-719.
24
Davies W J and Zhang J 1991 Root signals and the regulation of growth and
development of plants in drying soil. Annual Review of Plant Physiology and
Plant Molecular Biology 42, 55-76.
Dell B, Bartle J R and Tacey W H 1983 Root occupation and root channels of jarrah
forest subsoils. Australian Journal of Botany 31, 615-627.
Dell B and Havel J J 1989 The jarrah forest, an introduction. In The jarrah forest : a
complex Mediterranean ecosystem. Eds. B Dell, J J Havel and N Malajczuk. pp
1-10. Kluwer Academic Publishers, Dordrecht.
Dell B, Havel J J and Malajczuk N 1989 The jarrah forest: a complex Mediterranean
ecosystem. Kluwer Academic Publishers, Dordrecht.
Doley D 1967 Water relations of Eucalyptus marginata Sm. under natural conditions.
Journal of Applied Ecology 55, 597-614.
Eberbach P L and Burrows G E 2006 The transpiration response by four
topographically distributed Eucalyptus species, to rainfall occurring during
drought in south eastern Australia. Physiologia Plantarum 127, 483-493.
Enright N J and Lamont B B 1992 Survival, growth and water relations of Banksia
seedlings on a sand mine rehabilitated site and adjacent scrub-heath sites.
Journal of Applied Ecology 29, 663-671.
Fan S, Blake T J and Blumwald E 1994 The relative contribution of elastic and osmotic
adjustments to turgor maintenance of woody species. Physiologia Plantarum 90,
408-413.
Farrington P, Turner J V and Gailitis V 1996 Tracing water uptake by jarrah
(Eucalyptus marginata) trees using natural abundances of deuterium. Trees 11,
9-15.
Florence R G 1996 Ecology and silviculture of eucalypt forests. CSIRO Publishing,
Melbourne. pp. 413.
Fritts H C 1976 Tree rings and climate. Academic Press, London. pp. 567.
Futuyma D J and Moreno G 1988 The evolution of ecological specialisation. Annual
Review of Ecology and Systematics 19, 133-143.
Gilkes R J, Scholz G and Dimmock G M 1973 Lateritic deep weathering of granite.
Journal of Soil Science 24, 523-536.
Grant C D, Bell D T, Koch J M and Loneragan W A 1996 Implications of seedling
emergence to site restoration following bauxite mining in Western Australia.
Restoration Ecology 4, 146-154.
25
Grieve B J 1956 Studies in the water relations of plants. I. Transpiration of Western
Australian sclerophylls. Journal of the Proceedings of the Royal Society of
Western Australia 40, 15-30.
Grigg A M, Veneklaas E J and Lambers H 2008 Water relations and mineral nutrition
of closely related woody plant species on desert dunes and interdunes.
Australian Journal of Botany 56, 27-43.
Harris A C 1956 Regeneration of jarrah (Eucalyptus marginata). Australian Forestry 20,
54-62.
Hobbs R J and Cramer V A 2003 Natural ecosystems: pattern and process in relation to
local and landscape diversity in southwestern Australian woodlands. Plant and
Soil 257, 371-378.
Hobbs R J and Norton D A 1996 Towards a conceptual framework for restoration
ecology. Restoration Ecology 4, 93-110.
Jacobs M R 1955 Growth habits of the Eucalypts. Institute of Foresters of Australia,
Canberra. pp. 262.
Kew G A, Mengler F C and Gilkes R J 2007 Regolith strength, water retention and
implications for ripping and plant root growth in bauxite mine restoration.
Restoration Ecology 15, (Supplement) S54-S64.
Kimber P C 1974 The root system of jarrah (Eucalyptus marginata). pp 1-5. Forests
Department of Western Australia, Perth.
Koch J M 2007 Alcoa's mining and restoration process in south Western Australia.
Restoration Ecology 15, (Supplement) S11-S16.
Koch J M and Samsa G P 2007 Restoring Jarrah Forest trees after bauxite mining in
Western Australia. Restoration Ecology 15, (Supplement) S17-S25.
Koch J M and Ward S C 2005 Thirteen-year growth of jarrah (Eucalyptus marginata)
on rehabilitated bauxite mines in south-western Australia. Australian Forestry
68, 176-185.
Koch J M, Ward S C, Grant C D and Ainsworth G L 1996 Effects of bauxite mine
restoration operations on topsoil seed reserves in the jarrah forest of Western
Australia. Restoration Ecology 4, 368-376.
Kolb T E and Stone J E 2000 Differences in leaf gas exchange and water relations
among species and tree sizes in an Arizona pine-oak forest. Tree Physiology 20,
1-12.
26
Körner C and Cochrane P M 1985 Stomatal responses and water relations of Eucalyptus
pauciflora in summer along an elevation gradient. Oecologia 66, 443-455.
Kramer P J 1988 Challenging concepts regarding plant water relations. Plant, Cell and
Environment 11, 565-568.
Kramer P J and Boyer J S 1995 Water relations of plants and soils. Academic Press, San
Diego. pp. 495.
Lacey S T, Brennan P D and Parekh J 2001 Deep may not be meaningful: cost and
effectiveness of various ripping tine configurations in a plantations cultivation
trial in eastern Australia. New Forests 21, 231-248.
Lambers H, Chapin III F S and Pons T L 1998 Plant Physiological Ecology. Springer-
Verlag, New York. pp. 540.
Lambers H and Poorter H 1992 Inherent variation in growth rate between higher plants:
A search for physiological causes and ecological consequences. Advances in
Ecological Research 23, 187-261.
Levitt J 1972 Plant responses to environmental stresses. Academic Press, New York.
Lynch J 1995 Root architecture and plant productivity. Plant Physiology 109, 7-13.
Macfarlane C, White D A and Adams M A 2004 The apparent feed-forward response to
vapour pressure deficit of stomata in droughted, field-grown Eucalyptus
globulus Labill. Plant, Cell and Environment 27, 1268-1280.
Markesteijn L and Poorter L 2009 Seedling root morphology and biomass allocation of
62 tropical tree species in relation to drought- and shade-tolerance. Journal of
Ecology 97, 311-325.
McArthur W M 1991 Reference Soils of South-Western Australia. Department of
Agriculture, Western Australia, Perth.
Mengler F C, Kew G A, Gilkes R J and Koch J M 2006 Using instrumented bulldozers
to map spatial variation in the strength of regolith for bauxite mine floor
rehabilitation. Soil and Tillage Research 90, 126-144.
Merchant A, Callister A, Arndt S, Tausz M and Adams M 2007 Contrasting
physiological responses of six Eucalyptus species to water deficit. Annals of
Botany 100, 1507-1515.
Myers B A and Neales T F 1986 Osmotic adjustment, induced by drought in seedlings
of three Eucalyptus species. Australian Journal of Plant Physiology 13, 597-603.
27
Nadeau L B and Pluth D J 1997 Spatial distribution of lodgepole pine and white spruce
seedling roots 10 years after deep tillage of a gray luvisol. Canadian Journal of
Botany 27, 1606-1613.
Ngugi M R, Doley D, Hunt M A, Dart P and Ryan P 2003 Leaf water relations of
Eucalyptus cloeziana and Eucalyptus argophloia in response to water deficit.
Tree Physiology 23, 335-343.
Nicholls J W P 1974 Effect of prescribed burning in a forest on wood characteristics of
jarrah. Australian Forestry 36, 178-189.
Niinemets Ü 2002 Stomatal conductance alone does not explain the decline in foliar
photosynthetic rates with increasing tree age and size in Picea abies and Pinus
sylvestris. Tree Physiology 22, 515-535.
Passioura J B 2002 'Soil conditions and plant growth'. Plant, Cell and Environment 25,
311-318.
Pate J and Dixon K 1996 Convergence and divergence in the south-western Australian
flora in adaptations of roots to limited availability of water and nutrients, fire
and heat stress. In Gondwanan heritage: past, present and future of the Western
Australian biota. Eds. S Hopper, J Chappill, M Harvey and A George. pp 249-
258. Surrey Beatty, Sydney.
Pate J S and Dawson T E 1999 Assessing the performance of woody plants in uptake
and utilisation of carbon, water and nutrients: implications for designing
agricultural mimic systems. Agroforestry Systems 45, 245-275.
Pate J S, Dieter Jeschke W, Dawson T E, Raphael C, Hartung W and Bowen B J 1998
Growth and seasonal utilisation of water and nutrients by Banksia prionotes.
Australian Journal of Botany 46, 511-532.
Pook E W, Costin A B and Moore C W E 1966 Water stress in native vegetation during
the drought of 1965. Australian Journal of Botany 14, 257-267.
Poot P and Lambers H 2003 Are trade-offs in allocation pattern and root morphology
related to species abundance? A congeneric comparison between rare and
common species in the south-western Australian flora. Journal of Ecology 91,
58-67.
Poot P and Lambers H 2008 Shallow-soil endemics: adaptive advantages and
constraints of a specialized root-system morphology. New Phytologist 178, 371-
381.
28
Prior L D and Eamus D 1999 Seasonal changes in leaf water characteristics of
Eucalyptus tetrodonta and Terminalia ferdinandiana saplings in a northern
Australian savanna. Australian Journal of Botany 47, 587-599.
Prior L D, Eamus D and Duff G A 1997 Seasonal and diurnal patterns of carbon
assimilation. stomatal conductance and leaf water potential in Eucalyptus
tetrodonta saplings in a wet-dry savanna in northern Australia. Australian
Journal of Botany 45, 241-258.
Rokich D P, Meney K A, Dixon K W and Sivasithamparam K 2001 The impact of soil
disturbance on root development in woodland communities in Western
Australia. Australian Journal of Botany 49, 169-183.
Rust S and Roloff A 2002 Reduced photosynthesis in old oak (Quercus robur): the
impact of crown and hydraulic architecture. Tree Physiology 22, 597-601.
Sadlier S B and Gilkes R J 1976 Development of bauxite in relation to parent material
near Jarrahdale, Western Australia. Journal of the Geological Society of
Australia 23, 333-334.
Schulze E D, Turner N C, Nicolle D and Schumacher J 2006 Leaf and wood carbon
isotope ratios, specific leaf areas and wood growth of Eucalyptus species across
a rainfall gradient in Australia. Tree Physiology 26, 479-492.
Shea S R, Hatch A B, Havel J J and Ritson P 1975 The effect of changes on forest
structure and composition on water quality and yield from the northern jarrah
forest. In Managing Terrestrial Ecosystems. Eds. J Kikkawa and H A Nix.
Proceedings of the Ecological Society of Australia.
Spoor G and Godwin R J 1978 An experimental investigation into the deep loosening of
soil by rigid tines. Journal of Agricultural Engineering Research 23, 243-258.
Stoate T N and Wallace W R 1938 Crown studies of jarrah saplings 1928-1938.
Australian Forestry 3, 64-73.
Stone E L and Kalisz P J 1991 On the maximum extent of tree roots. Forest Ecology
and Management 46, 59-102.
Stoneman G L and Dell B 1993 Growth of Eucalyptus marginata (jarrah) seedlings in a
greenhouse in response to shade and soil temperature. Tree Physiology 13, 239-
252.
Stoneman G L, Dell B and Turner N C 1995 Growth of Eucalyptus marginata (jarrah)
seedlings in Mediterranean-climate forest in south-west Australia in response to
29
overstorey, site and fertiliser application. Forest Ecology and Management 79,
173-184.
Stoneman G L, Turner N C and Dell B 1994 Leaf growth, photosynthesis and tissue
water relations of greenhouse-grown Eucalyptus marginata seedlings in
response to water deficits. Tree Physiology 14, 633-646.
Szota C, Veneklaas E J, Koch J M and Lambers H 2007 Root architecture of jarrah
(Eucalyptus marginata) trees in relation to post-mining deep ripping in Western
Australia. Restoration Ecology 15, (Supplement) S65-S73.
Tacey W H 1979a Landscaping and revegetation practices used in rehabilitation after
bauxite mining in Western Australia. Reclamation Review 2, 123-132.
Tacey W H 1979b Sub-soil preparation and nutrition effects on the early growth of
Eucalyptus species. Alcoa of Australia Limited Environmental Research
Bulletin No. 4., 1-9.
Tardieu F and Davies W J 1992 Stomatal response to ABA is a function of current plant
water status. Plant Physiology 98, 540-545.
Thomas D S and Eamus D 1999 The influence of predawn leaf water potential on
stomatal responses to atmospheric water content at constant Ci and on stem
hydraulic coductance and foliar ABA concentrations. Journal of Experimental
Botany 50, 243-251.
Turner D W 2006 An index of osmotic adjustment that allows comparison of its
magnitude across species and experiments Physiologia Plantarum 127, 478-482.
Turner N C and Jones M M 1980 Turgor maintenance by osmotic adjustment: a review
and evaluation. In Adaptation of plants to water and high temperature stress.
Eds. N C Turner and P J Kramer. pp 155-172. Wiley, New York.
Varelides C and Kritikos T 1995 Effect of site preparation intensity and fertilisation on
Pinus pinaster survival and height growth on three sites in northern Greece.
Forest Ecology and Management 73, 111-115.
Veneklaas E J and Poot P 2003 Seasonal patterns in water use and leaf turnover of
different plant functional types in a species-rich woodland, south-western
Australia. Plant and Soil 257, 295-304.
Ward S C and Koch J M 1995 Early growth of jarrah (Eucalyptus marginata Donn ex
Smith) on rehabilitated bauxite minesites in south-west Australia. Australian
Forestry 58, 65-71.
30
Ward S C, Koch J M and Ainsworth G L 1996 The effect of timing of rehabilitation
procedures on the establishment of a jarrah forest after bauxite mining.
Restoration Ecology 4, 19-24.
Warren C R, Bleby T M and Adams M A 2007 Changes in gas exchange versus leaf
solutes as a means to cope with summer drought in Eucalyptus marginata.
Oecologia 154, 1-10.
Whisenant S G 1999 Repairing damaged wildlands - a process-orientated, landscape-
scale approach. Cambridge University Press, Cambridge. pp. 324.
White D A, Turner N C and Galbraith J H 2000 Leaf water relations and stomatal
behaviour of four allopatric Eucalyptus species planted in Mediterranean
southwestern Australia. Tree Physiology 20, 1157-1165.
Whitford K R 2002 Hollows in jarrah (Eucalyptus marginata) and marri (Corymbia
calophylla) trees. I. Hollow sizes, tree attributes and ages. Forest Ecology and
Management 160, 201-214.
Wildy D T and Pate J S 2002 Quantifying above- and below-ground growth responses
of the Western Australian oil mallee, Eucalyptus kochii subsp. plenissima, to
contrasting decapitation regimes. Annals of Botany 90, 185-197.
Wildy D T, Pate J S and Bartle J R 2004a Budgets of water use by Eucalyptus kochii
tree belts in the semi-arid wheatbelt of Western Australia. Plant and Soil 262,
129-149.
Wildy D T, Pate J S and Sefcik L T 2004b Water-use efficiency of a mallee eucalypt
growing naturally and in short-rotation coppice cultivation. Plant and Soil 262,
111-128.
Zencich S J, Froend R H, Turner J V and Gailitis V 2002 Influence of groundwater
depth on the seasonal sources of water accessed by Banksia tree species on a
shallow, sandy coastal aquifer. Oecologia 131, 8-19.
31
Chapter 1: Root morphology of jarrah (Eucalyptus marginata) trees in
relation to post-mining deep-ripping in south-western Australia
Abstract
The aim of this research was to investigate the coarse root systems of jarrah (Eucalyptus
marginata) trees at a 13-year-old restored bauxite mine site in south-western Australia.
Tree excavations at a site with small trees (low-quality site) revealed that deep-ripping
equipment had failed to penetrate the cemented lateritic subsoil, causing coarse roots (roots
>5mm in diameter) to be restricted to the top 0.5 m of the soil profile, resulting in fewer
(1344 stems ha-1) and smaller (mean height 4.5 m) jarrah trees. An adjacent area within the
same pit (high-quality site) with a stand density of 3256 stems ha-1 and a mean tree height
of 8.0 m had a kaolinitic clay subsoil which coarse roots were able to penetrate to the
average ripping depth of 1.5 m. Trees at the low-quality site did not penetrate the subsoil
with their taproot and instead relied on a large number of lateral roots (8.0 and 5.3 per tree)
and sinker roots (16.5 and 12.0 per tree). The taproots of trees on crests at the high-quality
site also did not penetrate the subsoil, and in contrast to trees at the low-quality site,
produced fewer lateral and sinker roots (2.3 and 2.0 per tree). The taproots of trees in
riplines at the high-quality site directly penetrated the ripline and these trees also produced
fewer lateral and sinker roots (5.0 and 3.7 per tree) than trees at the low-quality site. Jarrah
trees appear to have opportunistic root systems with the ability to respond to a variety of
soil conditions encountered in the post-mining landscape.
Introduction
The jarrah (Eucalyptus marginata) forest is endemic to the Darling Plateau of south-
western Australia, and occurs on deep lateritic soil profiles created through in situ
weathering of mainly granitic parent material (Sadlier and Gilkes 1976; Churchward and
Dimmock 1989). The lateritic soils of the Darling Plateau are rich in aluminium hydroxide
minerals, which are mined as bauxite (McArthur 1991). Bauxite mining is a major industry
in the region; with approximately 550 ha of jarrah forest mined and restored by Alcoa
World Alumina Australia each year (Koch 2007). The aim of Alcoa’s restoration process
since the early 1990s has been to create a sustainable jarrah forest with the pre-mining
32
values of the forest, including biodiversity, water production, timber resource and
recreation.
Techniques currently used in bauxite mine restoration such as direct-return of
topsoil, broadcast seeding, fertiliser application and deep-ripping of subsoil are largely
successful at rapidly establishing vegetation across the landscape (Grant et al. 1996; Koch
et al. 1996; Ward et al. 1996). However, despite identical restoration practices in all pits,
some areas of poor tree growth appear several years after establishment.
Soil profiles in post-mining areas are heterogeneous and contain a range of
regolithic materials that, due to their nature as well as the influence of mining, can prevent
tree root penetration (Mengler et al. 2006; Kew et al. 2007). Previous studies on
rehabilitated bauxite mines in south-western Australia have found that the root systems of
young, eastern-Australian eucalypt species were restricted to friable soil in riplines (Shea et
al. 1975; Tacey 1979; Dell et al. 1983). Roots can be confined to riplines following deep-
ripping operations as a result of poor soil loosening and localized compaction caused by the
ripping tine (Spoor and Godwin 1978). Deep-ripping on the whole, however, does increase
survival and height for a range of tree species on a number of different soil types in a
number of contrasting environments (Varelides and Kritikos 1995; Ashby 1997; Nadeau
and Pluth 1997; Lacey et al. 2001).
To survive the summer drought, mature jarrah trees rely on vertical roots that pass
through fissures in the lateritic duricrust and mottled zone, and access water-holding
kaolinitic clay deep in the pallid zone and saprolite above the bedrock (Doley 1967; Kimber
1974; Carbon et al. 1980; Dell et al. 1983; Farrington et al. 1996). If tree roots are unable
to penetrate deeper soil layers, the trees may have a reduced tolerance to long periods of
drought (Ashby 1997).
The purpose of the present study was to determine the cause(s) of poor growth and
poor survival in areas of a rehabilitated pit where tree establishment and growth was highly
variable. It is expected that poor tree growth in older areas (>10 years old) is caused by
restriction of root growth by impenetrable subsoil materials. This study aimed to describe
and quantify coarse root system morphologies that have developed in response to different
soil conditions encountered in the post-mining environment.
33
Materials and Methods
Study site
This study was carried out in a 13-year-old restored bauxite mine pit, located approximately
10 km north-west of Dwellingup (32º43´S, 116º04´E), Western Australia, Australia. In this
study, two plots (each measuring 25 m x 50 m) were marked out with the first in a patch of
small trees, subjectively classed as low-quality, and the second in an adjacent area of taller
trees (high-quality area) within the same restored pit (Fig. 1.1). The study site was
originally selected using aerial photographs followed by ground checks to ensure that the
variation in tree height was not due to human interference since initial post-mining
restoration. Mining and restoration records of the area were also consulted to confirm that
no atypical disturbance to the area was caused during mining, and that the area had not
previously been used for research trials.
Figure 1.1. Photographs of low-quality (left) and high-quality (right) restored jarrah
(Eucalyptus marginata) forest sites used in this study. The white stick is 2 m long.
Photographs by J. Koch.
34
The study area was restored according to the following general procedure used at
the time (1992). Mine pit walls were smoothed down to create more natural contours and
blend the pit into the surrounding landscape. Sandy gravel (overburden) was spread over
the mine floor to a depth of approximately 0.5 m. Fresh topsoil (direct-return) was spread
over the returned overburden to a depth of 0.1 m. The site was then deep-ripped using a
Caterpillar D11 bulldozer with a single tine with 60 cm wings capable of ripping to a depth
of 1.5 m; with 2 m spacing between riplines. The ripping produced crests and riplines with
approximately half of the final surface being crests and half riplines (Fig 1.2). Seeds were
broadcast, at rates based on pre-mining vegetation surveys, following break-of-season
rainfall in autumn. The seed mixture was designed to produce a tree stand density of 2500
stems ha-1 with 80% jarrah and 20% marri (Corymbia calophylla). Nitrogen and
phosphorus fertilizers were applied in spring. For details of current mining and restoration
processes, see Koch (2007).
Stand characteristics
Stand characteristics were measured at both sites in May, 2003. Stand density was
determined by counting all jarrah trees greater than 2 m tall in the 1250 m2 plots. Tree
height was measured for all jarrah trees >2 m tall at both sites, and recorded as the height of
the tallest living section of the crown. Girth over bark at breast height (1.3 m) was
recorded for all stems of all jarrah trees >2 m tall at both sites, and converted to basal area
over bark at breast height (BA). In the case of multi-stemmed trees, total tree BA was
calculated as the sum of the BA of each stem >2 m tall. The location (crest or ripline) of
each tree was also recorded.
Soil texture and bulk density
Three soil pits were dug amongst the excavated trees at each site, perpendicular to the
ripline direction. Soil texture was determined through field texturing and observations of
material using a hand lens (McDonald and Isbell 1998). Soil colour was classified using
Munsell soil colour charts (Munsell Color Company Inc., Baltimore, USA). In each soil
pit, bulk density samples were taken from both crests and riplines using brass soil cores
with a volume of 280 cm3. Bulk density samples were taken at 10 cm intervals to depths of
35
approximately 1 m in the low-quality site, and 1.6 m at the high-quality site which were the
maximum depths achievable. Due to the large proportion of rocks encountered, several
attempts were required to retrieve complete samples. Complete samples were transferred to
zip-lock bags in the field then taken to the laboratory for analysis. In the laboratory, the
samples were transferred into aluminium dishes and then oven-dried at 105ºC for 12 hours.
Dry weights of the samples were taken, and bulk density calculated as dry weight of the
sample divided by the volume of the sampling core. Samples were then passed through a
2-mm sieve to determine gravel content.
Figure 1.2. Diagram of the depth of soil horizons at low-quality (left) and high-quality (right) restored jarrah (Eucalyptus marginata) forest sites. Scale bars represent depth (m) as measured from the soil surface of crests (left-hand scale bars) and riplines (right-hand scale bars) for both soil profiles.
Crest Ripline
Mottled Zone
Low Quality Site
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Crest Ripline
Topsoil
Sandy Gravel / Clay Mixture
Clay
High Quality Site
Sandy Gravel
Topsoil
Sandy Gravel
0
0.2
0.4
0.6
0.8
1.0
1.2
0
0.2
0.4
0.6
0.8
1.0
Crest Ripline
Mottled Zone
Low Quality Site
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
Crest Ripline
Topsoil
Sandy Gravel / Clay Mixture
Clay
High Quality Site
Sandy Gravel
Topsoil
Sandy Gravel
0
0.2
0.4
0.6
0.8
1.0
1.2
0
0.2
0.4
0.6
0.8
1.0
36
Tree root morphology
Six trees in the median-height size class of each site were excavated to study coarse root
(>5 mm in diameter) distribution. The median-height class was 4-5 m in the low-quality
site, and 8-9 m in the high-quality site. Within each site, three trees were situated on crests
and the remaining three situated in riplines. The coarse root system (all roots >5 mm in
diameter) of each tree was excavated manually using a mattock and then a rock pick for
finer work in order to minimize damage. Excavations focused on exposing the taproot
(vertical root emerging from the base of the tree) as well as lateral (horizontal roots
emerging from the base of the tree) and sinker (vertical roots emerging from lateral roots)
roots. The depth of excavation depended on the length of vertical roots (taproot and sinker
roots). Due to hardness of the material, the maximum depth attainable was approximately 1
m on the low-quality site, and 1.6 m on the high-quality site. This depth was more than
adequate to trace coarse vertical roots to their end point at the low-quality site. Some fine
roots (<5 mm in diameter) in riplines in the high-quality site continued beyond 1.6 m depth;
therefore, root depth recorded was the depth achieved by coarse roots.
Root girth over bark was measured at regular intervals along the length of the root.
Lateral root girth was measured at 0, 0.2, 0.5, 1, 1.5, 2, 2.5 and 3 m from the base of the
tree. Sampling to 3 m maximum distance along lateral roots allowed the inclusion of all
sinker roots. Previous studies on jarrah poles (10-30 year old trees) found that the majority
of sinkers occurred within 1 m of the root stock, with no sinker roots more than 3 m from
the base of the tree (Kimber 1974). Sinker root and taproot girth was measured at 0, 0.2,
0.5 and 1 m depth from the soil surface. Sinker root girth was also measured at these
standard distances from the lateral root/sinker root junction. The distance of sinker root
emergence from the tree was recorded, as well as whether the sinker root emerged on a
crest or in a ripline. Lateral root girth was also measured on both sides of lateral/sinker root
junctions. For comparisons between sites (low-quality and high-quality) and situations (on
crest or in ripline); girth was converted to diameter or cross-sectional area (CSA).
Root cross-sectional area allocation calculations
As a standardized measure, unaffected by tree size, the relative importance of different root
types was calculated as a percentage of total root cross-sectional area (CSA); similar to the
method used by Drexhage & Gruber (1998). Root CSA was measured at 2 m from the
37
trunk for lateral roots, and at 0.5 m depth for sinker and taproots. A 2-m radius from the
trunk for laterals was used in order to include all sinker roots in the calculation, as all
sinkers emerged within 2 m of the tree. A depth of 0.5 m depth was selected so as to
include sinker cross-sectional area in all situations, as sinkers were not present below 0.5 m
with the exception of sinkers in riplines at the high-quality site. Measuring lateral root
CSA at 2 m rather than closer to the trunk yields lower estimates for the allocation to lateral
roots, but ensures that the calculated total lateral root CSA only includes functionally
horizontal surface roots, and does not include a proportion of sinker roots.
Data analyses
As the number of trees at each site (low-quality and high-quality) and in each situation
(crest and ripline) was different, significant differences in mean tree height and basal area
were determined using a one-way analysis of variance (ANOVA) with no blocking using
GenStat (v. 7.1). Similarly, as the total number of lateral and sinker roots differed between
trees at each site and in each situation, one-way ANOVAs with no blocking were also used
to determine significant differences in taproot and sinker root depth. Differences in soil
bulk density and gravel content, as well as differences in average lateral, sinker and taproot
diameters were tested at each depth sampled also with one-way ANOVAs. Differences
between treatments with regard to proportion of total root CSA accounted for by each root
type were also tested using a one-way ANOVA. All data were tested for normality using a
Shapiro-Wilk test and log- or arcsine-transformations were performed where appropriate).
Results
Stand characteristics
The low-quality site had less than half the number of trees of the neighbouring high-quality
site and approximately 60% of trees at both sites were located in riplines (Table 1.1). Trees
on crests and in riplines at the low-quality site were ~40% shorter (P<0.001) and had 13-
47% less basal area (P<0.001) than those at the high-quality site. There was no significant
difference in either height or basal area between trees growing on crests or in riplines at the
low-quality site. Trees growing on crests at the high-quality site, however, were 10%
shorter (P<0.001) and had 26% less basal area (P<0.001) than trees growing in riplines.
38
Table 1.1. Number of trees in plot (1250 m2), mean height (±SE) and mean basal area per tree (±SE) at breast height (1.3 m) of jarrah (Eucalyptus marginata) trees at low-quality and high-quality restored bauxite mine sites. Values are further categorised into whether trees were situated on a crest or in a ripline within each site. Within rows, different letters indicate significant differences (P=0.05). Site Low-quality Low-quality High-quality High-quality
Tree situation Crest Ripline Crest Ripline P-value
Number of trees 70 98 160 247
Height (m) 4.6 ± (0.2)a 4.5 (±0.1)a 7.5 (±0.2)b 8.3 (±0.1)c <0.001
Basal Area (cm2) 95.0 (±9.0)a 77.7 (±5.6)a 109.6 (±6.5)b 148.4 (±6.4)c <0.001
Soil texture, gravel content and bulk density
Both sites had similar upper soil layers (Fig. 1.2). Both had 15-20 cm of topsoil (dark-
brown, sandy loam; 10YR3/3; 60-70% gravel) and 20-35 cm of sandy gravel (strong brown
7.5YR5/8 to yellowish brown 10YR5/8 sandy loam; 70-90% gravel) above the previous
mine floor. The difference in height between the soil surface on crests and in riplines was
20-25 cm at the low-quality site and 10-15 cm at the high-quality site. The distance
between riplines and their nearest crest was 1-1.2 m in the area sampled at both sites.
At approximately 0.5 m depth at the low-quality site was a cemented layer of
mottled zone material; composed mainly of sandy loam soil, gravel and large rocks. This
material had no large cracks or fissures in the area excavated and no roots were found to
penetrate the cemented mottled zone layer. The cemented layer was flat and continuous,
and therefore the depth of soil situated above it depended on whether samples were taken
from riplines or crests (Fig. 1.2). It appears the deep ripper was unable to penetrate this
material, and that the ripping tine simply dragged on top of the cemented layer.
Below 0.5 m at the high-quality site was a mixed horizon of sandy gravel
(overburden) and kaolinitic clay (white silty clay 10YR8/2), caused by the ripping process.
Under crests, this layer was only 5-10 cm deep and often hard to distinguish. Under
riplines, this mixed zone was up to 1 m deep, such that the ripped zone extended to
approximately 1.2-1.5 m below the soil surface. Beneath the ripped zone was a kaolinitic
white clay horizon that continued below excavation depth (approximately 1.6 m).
39
Although difficult to distinguish in some cases, the width of the ripped zone was
approximately 1 m.
Bulk density and gravel content results were highly variable due to the
heterogeneous nature of the soil profile. Bulk densities were not significantly different for
the majority of sampling depths (Fig. 1.3A and 1.3B). Soil under crests had higher gravel
contents at both sites (P<0.001), however, this difference only occurred for samples taken
from the surface layers (Fig. 1.3C and 1.3D).
Taproot and sinker root depth
Taproots and sinker roots located on crests and in riplines at the low-quality site achieved
an average depth of ~0.6 m and those on crests in the high-quality site reached an average
depth of ~0.5 m (Table 1.2). Both distances were less than that from the soil surface to the
level of the original mine floor. Taproots and sinker roots located in riplines at the high-
quality site accessed the subsoil in the riplines to a depth of 1.3-1.6 m, however, they did
not penetrate below the ripping depth (~1.3-1.6 m).
Table 1.2. Total number of sinker roots in each location (crest or ripline) for twelve jarrah (Eucalyptus marginata) trees excavated at low-quality and high-quality restored bauxite mine sites; as well as mean depth (± SE) achieved by sinker roots (n=‘total sinker number’) and taproots (n=3) initiating on crests and in riplines at low-quality and high-quality sites. Within rows, different letters indicate significant differences (P=0.05).
Site Low-quality Low-quality High-quality High-quality
Root location Crest Ripline Crest Ripline P-value
Sinker number 23 38 10 7
Sinker depth (m) 0.58 (±0.01)b 0.61 (±0.01)b 0.48 (±0.02)a 1.53 (±0.05)c <0.001
Taproot depth (m) 0.64 (±0.03)c 0.61 (±0.07)b 0.52 (±0.02)a 1.52 (±0.06)d <0.001
40
Figure 1.3. Mean (±SE) soil bulk density (A and B) and mean (±SE) gravel content (C and D) with increasing depth (m) on crest (squares) and adjacent ripline (circles) soil profiles at low-quality (A and C) and high-quality (B and D) restored jarrah (Eucalyptus marginata) forest sites. Bars represent standard error (n=3). Bold bars represent least significant difference (l.s.d.) at each depth sampled. Samples from the low-quality site were not taken below 1 m depth.
Root number and location
Trees differed in their average number of lateral and sinker roots, both within and between
sites (Table 1.3). At the low-quality site, trees located on crests averaged 8.0 lateral roots
while those in riplines averaged 5.3 lateral roots per tree (P=0.002). At the high-quality
site, trees located on crests averaged 2.3 lateral roots while those in riplines averaged 5.0
lateral roots per tree (P=0.002).
Trees on crests and in riplines at the low-quality site had significantly more sinker
roots (P<0.001) than those at the high-quality site (Table 1.3). The percentage of sinker
roots that were in riplines did not vary significantly between trees on crests or in riplines at
either site. There was also no significant difference in the average distance from the tree
that sinker roots emerged on crests or in riplines at both sites.
-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 20 40 60 80 100Gravel content (%)
Soi
l dep
th (m
)
-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 0.5 1 1.5 2 2.5Soil bulk density (g cm-3)
Soi
l dep
th (m
)
-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 20 40 60 80 100Gravel content (%)
Soi
l dep
th (m
)-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 0.5 1 1.5 2 2.5Soil bulk density (g cm-3)
Soi
l dep
th (m
)A
DB
C
-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 20 40 60 80 100Gravel content (%)
Soi
l dep
th (m
)
-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 0.5 1 1.5 2 2.5Soil bulk density (g cm-3)
Soi
l dep
th (m
)
-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 20 40 60 80 100Gravel content (%)
Soi
l dep
th (m
)-1.6-1.4-1.2
-1-0.8-0.6-0.4-0.2
0
0 0.5 1 1.5 2 2.5Soil bulk density (g cm-3)
Soi
l dep
th (m
)A
DB
C
41
Table 1.3. Mean number of lateral and sinker roots per tree, percentage of sinker roots located in riplines and mean distance of sinker roots from the base of jarrah (Eucalyptus marginata) trees situated on crests and in riplines at low-quality and high-quality restored bauxite mine sites. Results are the mean (±SE) of 3 trees per site/situation (n=3). Within rows, different letters indicate significant differences (P=0.05).
Site Low-quality Low-quality High-quality High-quality
Tree situation Crest Ripline Crest Ripline P-value
Laterals per tree 8.0 (±0.6)c 5.3 (±0.7)b 2.3 (±0.7)a 5.0 (±0.6)b 0.002
Sinkers per tree 16.5 (±4.6)c 12.0 (±0.8)b 2.0 (±1.7)a 3.7 (±0.3)a <0.001
% sinkers in riplines 63.3 (±12.6)a 59.4 (±10.8)a 75.0 (±25.0)a 36.1 (±7.3)a n.s.
Dist. from base (m) 0.87 (±0.09)a 1.05 (±0.12)a 0.98 (±0.18)a 0.56 (±0.09)a n.s.
Root size
Lateral root size was significantly different between sites at each distance measured;
however, there was no difference between trees on crests and in riplines within sites (Fig.
1.4). Lateral roots of trees on the low-quality site were 30-40% smaller (P<0.001) than
those at the high-quality site at the root origin.
The average diameter of sinker roots was dependent on their location in the
landscape, regardless of where the tree was situated (Fig. 1.5A). Sinker roots originating
on crests and in riplines at the low-quality site, as well as those on crests at the high-quality
site were 45-70% smaller (P<0.001) than sinker roots located in riplines at the high-quality
site at depths of 0, 0.2 and 0.5 m. Only sinker roots in riplines at the high-quality site
penetrated past 0.6 m (Table 1.2), and therefore only these roots were present at 1 m (Fig.
1.5A). Taproots of trees located on crests and in riplines at the low-quality site, as well as
those on crests at the high-quality site were 72-82% smaller (P<0.001) than those of trees
in riplines at the high-quality site at 0.5 m depth (Fig. 1.5B). Taproots in riplines at the
high-quality site were the only ones that penetrated deeper than 0.6 m (Table 1.2). There
was no significant difference between the size of taproots at ground level or at 0.2 m depth
(Fig. 1.5B).
42
Figure 1.4. Mean diameter of lateral roots of jarrah (Eucalyptus marginata) with increasing distance from the base of the tree for trees situated on crests (squares) and in riplines (circles) at low-quality (solid) and high-quality (open) restored bauxite mine sites. Bars represent standard error (only positive bars shown). Bold bars represent least significant difference (l.s.d.) at each distance from the base of the tree sampled.
Figure 1.5. Mean diameter of sinker roots (A) and taproots (B) of jarrah (Eucalyptus marginata) with increasing soil depth of trees on crests (squares) and in riplines (circles) at low-quality (solid) and high-quality (open) restored bauxite mine sites. Only sinker roots and taproots of jarrah trees situated in riplines at the high-quality site were present at 1 m depth. Bars represent standard error. Bold bars represent least significant difference (l.s.d.) at each depth sampled.
Allocation to root type
The taproots of trees on crests and in riplines at the low-quality site, as well as those on
crests at the high-quality site constituted 22-26% of total root CSA (Fig. 1.6), while
taproots of trees in riplines at the high-quality site represented 76% of their total root CSA
(P=0.012).
0
20
40
60
80
100
0 1 2 3Distance from tree (m)
Dia
met
er (m
m)
-1.0
-0.8
-0.6
-0.4
-0.2
0.00 100 200 300
Diameter (mm)
Soi
l dep
th (m
)
-1.0
-0.8
-0.6
-0.4
-0.2
0.00 10 20 30 40 50
Diameter (mm)
Soi
l dep
th (m
)
A B-1.0
-0.8
-0.6
-0.4
-0.2
0.00 100 200 300
Diameter (mm)
Soi
l dep
th (m
)
-1.0
-0.8
-0.6
-0.4
-0.2
0.00 10 20 30 40 50
Diameter (mm)
Soi
l dep
th (m
)
A B
43
Sinker roots of trees on crests and in riplines at the low-quality site, as well as those
on crests at the high-quality site accounted for 33-47% of total root CSA compared with
less than 10% for trees in riplines at the high-quality site (P<0.05). There was no
significant difference between trees in the total root CSA accounted for by lateral roots
(Fig. 1.6).
Figure 1.6. Mean proportion of total root cross-sectional area accounted for by lateral (black), sinker (grey) and taproots (white) for jarrah (Eucalyptus marginata) trees situated on crests and in riplines at low-quality (LQ) and high-quality (HQ) restored forest sites. Bars represent standard error. Within each root type, bars with different letters represent significant differences (P=0.05).
While trees on crests at the low-quality site and trees from the high-quality site were
similar in the proportion of total root CSA accounted for by each root type, they differed
significantly in the number and size of roots they produced. The largest lateral root of trees
at the low-quality site and trees in riplines at the high-quality site accounted for
approximately 30% of the total CSA allocated to lateral roots (Fig. 1.7). Trees on crests at
the high-quality site differed significantly in that their largest lateral root accounted for
more than 80% of the total amount of lateral CSA (P<0.001). Similarly, the largest sinker
root of trees on crests at the high-quality site accounted for more than 80% of their total
sinker root CSA, compared with trees in all other situations which had a more even
allocation amongst their sinker roots (P<0.001).
0
20
40
60
80
100
LQ Crest LQ Rip HQ Crest HQ RipSite and situation
Roo
t typ
e (%
)
ns
a aa
aa
a
b
b
nsns ns
0
20
40
60
80
100
LQ Crest LQ Rip HQ Crest HQ RipSite and situation
Roo
t typ
e (%
)
ns
a aa
aa
a
b
b
nsns ns
44
Figure 1.7. Mean largest representative of lateral (black) and sinker (grey) roots expressed as a percentage of the total allocation of root cross-sectional area to that root type for jarrah (Eucalyptus marginata) trees excavated at low-quality (LQ) and high-quality (HQ) restored forest sites. Taproot results are not included as all trees had only one taproot at the root origin. Bars represent standard error (n=3). Within each root type, bars with different letters indicate significant differences (P=0.05).
Discussion
Tree productivity as a function of soil texture, deep-ripping and coarse root depth
The above-ground differences between low- and high-quality sites were a direct result of
both the depth achieved by vertical roots (taproots and sinker roots) and the contrasting
nature of the subsoil materials at each site. Above-ground growth at the low-quality site
was half that achieved by restored sites of similar age (Koch and Ward 2005; Koch and
Samsa 2007). Deep-ripping failed to break through the cemented lateritic subsoil at the
low-quality site, resulting in a restriction of coarse roots to upper soil layers. It is unlikely
that such material can be improved as a medium for root growth using the current single-
pass ripping operation (Mengler et al. 2006; Kew et al. 2007)
It is likely that the restriction of roots to the sandy gravel soil in the top 0.5-0.6 m at
the low-quality site will cause these trees to experience water stress much earlier in summer
(see Chapter 3) compared with those at the high-quality site. The restriction of root
systems is the most likely cause of reduced stand density and tree size at the low-quality
site. In contrast, trees at the high-quality site were larger as riplines facilitated access to the
subsoil; allowing them access to a larger soil volume and a soil texture with a larger
capacity to store moisture (Carbon et al. 1980; McArthur 1991). A number of tree species
have shown a similar trend in response to deep-ripping (Varelides and Kritikos 1995;
0
20
40
60
80
100
LQ Crest LQ Rip HQ Crest HQ RipSite and situation
Larg
est r
oot (
%)
aa
aa
b
a a
b
0
20
40
60
80
100
LQ Crest LQ Rip HQ Crest HQ RipSite and situation
Larg
est r
oot (
%)
aa
aa
b
a a
b
45
Nadeau and Pluth 1997; Lacey et al. 2001); including those regarded as having the ability
to grow well on compacted soils (Ashby 1997).
All coarse roots that penetrated the subsoil at the high-quality site were restricted to
riplines; a result consistent with previous studies on rehabilitated bauxite mines (Shea et al.
1975; Dell et al. 1983). Shea et al. (1975) commented that the trees in their study were
only three years old, and expected that they would penetrate the clay matrix below the
ripline as they developed. Dell et al. (1983) studied these same species when the trees were
6-8 years old, and found that roots remained restricted to the returned soil layers and in the
rip fracture zone on granite-based rehabilitated profiles. While no coarse roots penetrated
below the ripping depth in the present study, some fine roots penetrated below the ripping
depth via soil ped faces.
The restriction of coarse roots to friable subsoil in riplines may be due to the effect
of ripping on soil structure, rather than inadequate ripping depth. Ripping moist clay can
have a moulding rather than a shattering effect on soil structure, which could potentially
result in localized compaction (Spoor and Godwin 1978; Mengler et al. 2006; Kew et al.
2007) causing roots to remain in the ripline. Chemical agents such as gypsum might be
used in conjunction with ripping to improve soil structure at the rip edge and below the
ripping depth. Coarse roots on unmined profiles access clay subsoil through natural root
channels (Dell et al. 1983), however, no natural root channels were observed during
excavations in the present study.
Tree root distribution in response to soil texture and deep-ripping
The relatively friable soil under trees located in riplines at the high-quality site facilitated
the taproot of these trees to penetrate the subsoil, while the taproots of trees located on
crests did not penetrate the old mine floor. Instead of a taproot, trees on crests at the high-
quality site had one large sinker root supported by one large lateral root which indicates a
tendency for jarrah to develop a single large vertical root where possible. The total sinker
root CSAs of these large sinkers were, however, far lower than the taproot CSA of trees in
riplines, which may explain why trees in riplines were taller and had a larger basal area
than trees on crests at the high-quality site. Trees at the low-quality site also lacked a
taproot; however, they produced a greater number of smaller lateral and sinker roots. The
46
production of a large number of sinker roots per tree at the low-quality site may be due to
the first sinker roots produced being unable to penetrate the subsoil; thereby triggering the
development of more sinker roots along the length of the lateral root. The fact that these
sinker roots were small as well as numerous indicates that once roots were unable to
penetrate the subsoil, their growth stopped and resources were diverted (Thaler and Pagès
1999) to the growth of other sinker roots further along the lateral root; also demonstrated by
coniferous species. This regular pattern of root development, similar to that observed for
Norway spruce (Picea abies) (Drexhage and Gruber 1998), may also explain why trees on
crests at the high-quality site only developed one major sinker root originating from one
major lateral root. Many species have demonstrated the ability to alter the allocation of
resources to different root types in response to physical barriers to growth (Enright and
Lamont 1992; Misra and Gibbons 1996; Drexhage and Gruber 1998; Rokich et al. 2001;
Poot and Lambers 2003; 2008). With regard to eucalypts in particular, Misra and Gibbons
(1996) found that Eucalyptus nitens, grown in pots with high soil strength throughout,
produced fewer, but longer, lateral roots, thus increasing the chance of finding more
favourable soil away from the base of the plant.
Loss of the taproot is not necessarily detrimental to jarrah tree survival. Kimber
(1974) found no evidence to suggest that jarrah must have a well-developed taproot, but did
conclude that factors such as slope, large boulders and shallowness of the gravel layer
influenced root-system structure. Many conifers are able to develop different root system
morphologies including taproot-dependant, sinker root-dependant, superficial and plate-
root systems in response to different soil conditions (Gruber 1994; Drexhage and Gruber
1998). The results from trees in the present study indicate that a single large taproot at
depth is an advantage for trees on rehabilitated soil profiles. Production of a single, large,
taproot on an unmined profile would not be an advantage in most cases. In order to
maintain growth and survive the summer drought, taproots and sinker roots of mature jarrah
trees in the unmined forest must pass through fissures in the lateritic duricrust and root
channels in the mottled and pallid zones in order to access water at depth (Kimber 1974;
Dell et al. 1983). Roots of radiata pine (Pinus radiata) have also been observed to access
deeper soil via friable soil in old root channels and fissures in order to access stored
moisture deep in the profile (Greenwood et al. 1981; Nambiar and Sands 1992).
47
Considering that trees in riplines at the high-quality site were taller and had larger
basal areas, it is likely that they will out-compete trees on crests as the stand matures
(Florence 1996). The root-system structure of trees on crests may also affect survival of
these trees. Using a high proportion of lateral allocation for sinker-root production
potentially reduces the root CSA available for surface nutrient and water uptake.
Furthermore, nutrient uptake is restricted to the direction of the single major lateral, so
these trees may exhaust their nutrient supply compared with trees that have many laterals
foraging in a larger soil volume. The reduced anchorage of trees on crests, due to the
asymmetry of their lateral roots and the loss of their taproot, may also make them more
susceptible to windthrow (Coutts 1983; Mickovski and Ennos 2002).
Conclusions
It is important to acknowledge that, due to the difficulty encountered in excavating tree
roots, the number of individuals sampled was low. Deep-ripping techniques used during
bauxite mine restoration vastly improve vegetation establishment on the whole (Shea et al.
1975), with the majority of restored sites able to support trees at high stocking densities
(Koch and Ward 2005). Due to the naturally variable soils of south-western Australia, it is
difficult to predict where and how often hostile subsoils will emerge on restored bauxite
mines, and even harder to predict the long-term impacts on the restored vegetation. From
the present study, it seems that jarrah trees are able to develop a range of different root
system morphologies in response to variable soil conditions encountered on restored
bauxite mine sites. Further studies on the functionality of these different root system
morphologies and how they influence tree growth and survival will greatly improve
methods of jarrah forest restoration.
References
Ashby W C 1997 Soil ripping and herbicides enhance tree and shrub restoration on
stripmines. Restoration Ecology 5, 169-177.
Carbon B A, Bartle G A, Murray A M and Macpherson D K 1980 The distribution of root
length, and the limits to flow of soil water to roots in a dry sclerophyll forest. Forest
Science 26, 656-664.
48
Churchward H M and Dimmock G M 1989 The soils and landforms of the northern jarrah
forest. In The jarrah forest: a complex Mediterranean ecosystem. Eds. B Dell, J J
Havel and N Malajczuk. pp 13-21. Kluwer Academic Publishers, Dordrecht.
Coutts M P 1983 Root architecture and tree stability. Plant and Soil 71, 171-188.
Dell B, Bartle J R and Tacey W H 1983 Root occupation and root channels of jarrah forest
subsoils. Australian Journal of Botany 31, 615-627.
Doley D 1967 Water relations of Eucalyptus marginata Sm. under natural conditions.
Journal of Applied Ecology 55, 597-614.
Drexhage M and Gruber F 1998 Architecture of the skeletal root system of 40-year-old
Picea abies on strongly acidified soils in the Harz Mountains (Germany). Canadian
Journal of Forest Research 28, 13-22.
Enright N J and Lamont B B 1992 Survival, growth and water relations of Banksia
seedlings on a sand mine rehabilitated site and adjacent scrub-heath sites. Journal of
Applied Ecology 29, 663-671.
Farrington P, Turner J V and Gailitis V 1996 Tracing water uptake by jarrah (Eucalyptus
marginata) trees using natural abundances of deuterium. Trees 11, 9-15.
Florence R G 1996 Ecology and silviculture of eucalypt forests. CSIRO Publishing,
Melbourne. pp. 413.
Grant C D, Bell D T, Koch J M and Loneragan W A 1996 Implications of seedling
emergence to site restoration following bauxite mining in Western Australia.
Restoration Ecology 4, 146-154.
Greenwood E A N, Beresford J D and Bartle J R 1981 Evaporation for vegetation in
landscapes developing secondary salinity using the ventilated-chamber technique.
III. Evaporation from a Pinus radiata tree and the surrounding pasture in an
agroforestry plantation. Journal of Hydrology, 155-166.
Gruber F 1994 Morphology of coniferous trees: possible effects of soil acidification on the
morphology of Norway spruce and silver fir. In Effects of acid rain on forest
processes. Eds. D Godbold and A Hüttermann. pp 265-324. John Wiley & Sons
Inc., New York.
49
Kew G A, Mengler F C and Gilkes R J 2007 Regolith strength, water retention and
implications for ripping and plant root growth in bauxite mine restoration.
Restoration Ecology 15, (Supplement) S54-S64.
Kimber P C 1974 The root system of jarrah (Eucalyptus marginata). pp 1-5. Forests
Department of Western Australia, Perth.
Koch J M 2007 Alcoa's mining and restoration process in south Western Australia.
Restoration Ecology 15, (Supplement) S11-S16.
Koch J M and Samsa G P 2007 Restoring Jarrah Forest trees after bauxite mining in
Western Australia. Restoration Ecology 15, (Supplement) S17-S25.
Koch J M and Ward S C 2005 Thirteen-year growth of jarrah (Eucalyptus marginata) on
rehabilitated bauxite mines in south-western Australia. Australian Forestry 68, 176-
185.
Koch J M, Ward S C, Grant C D and Ainsworth G L 1996 Effects of bauxite mine
restoration operations on topsoil seed reserves in the jarrah forest of Western
Australia. Restoration Ecology 4, 368-376.
Lacey S T, Brennan P D and Parekh J 2001 Deep may not be meaningful: cost and
effectiveness of various ripping tine configurations in a plantations cultivation trial
in eastern Australia. New Forests 21, 231-248.
McArthur W M 1991 Reference Soils of South-Western Australia. Department of
Agriculture, Western Australia, Perth.
McDonald R C and Isbell R F 1998 Soil profile. In Australian soil and and survey field
handbook. Eds. R C McDonald, R F Isbell, J G Speight, J Walker and M S Hopkins.
Australian Collaborative Land Evaluation Program, CSIRO Land and Water,
Canberra.
Mengler F C, Kew G A, Gilkes R J and Koch J M 2006 Using instrumented bulldozers to
map spatial variation in the strength of regolith for bauxite mine floor rehabilitation.
Soil and Tillage Research 90, 126-144.
Mickovski S B and Ennos A R 2002 A morphological and mechanical study of the root
systems of suppressed crown Scots pine Pinus sylvestris. Trees 16, 274-280.
Misra R K and Gibbons A K 1996 Growth and morphology of eucalypt seedling-roots, in
relation to soil strength arising from compaction. Plant and Soil 182, 1-11.
50
Nadeau L B and Pluth D J 1997 Spatial distribution of lodgepole pine and white spruce
seedling roots 10 years after deep tillage of a gray luvisol. Canadian Journal of
Botany 27, 1606-1613.
Nambiar E K S and Sands R 1992 Effects of compaction and simulated foot channels in the
subsoil on root development, water uptake and growth of radiata pine. Tree
Physiology 10, 297-306.
Poot P and Lambers H 2003 Are trade-offs in allocation pattern and root morphology
related to species abundance? A congeneric comparison between rare and common
species in the south-western Australian flora. Journal of Ecology 91, 58-67.
Poot P and Lambers H 2008 Shallow-soil endemics: adaptive advantages and constraints of
a specialized root-system morphology. New Phytologist 178, 371-381.
Rokich D P, Meney K A, Dixon K W and Sivasithamparam K 2001 The impact of soil
disturbance on root development in woodland communities in Western Australia.
Australian Journal of Botany 49, 169-183.
Sadlier S B and Gilkes R J 1976 Development of bauxite in relation to parent material near
Jarrahdale, Western Australia. Journal of the Geological Society of Australia 23,
333-334.
Shea S R, Hatch A B, Havel J J and Ritson P 1975 The effect of changes on forest structure
and composition on water quality and yield from the northern jarrah forest. In
Managing Terrestrial Ecosystems. Eds. J Kikkawa and H A Nix. Proceedings of the
Ecological Society of Australia.
Spoor G and Godwin R J 1978 An experimental investigation into the deep loosening of
soil by rigid tines. Journal of Agricultural Engineering Research 23, 243-258.
Tacey W H 1979 Sub-soil preparation and nutrition effects on the early growth of
Eucalyptus species. Alcoa of Australia Limited Environmental Research Bulletin
No. 4., 1-9.
Thaler P and Pagès L 1999 Why are laterals less affected than main axes by homogeneous
unfavourable physical conditions? A model-based hypothesis. Plant and Soil 217,
151-157.
51
Varelides C and Kritikos T 1995 Effect of site preparation intensity and fertilisation on
Pinus pinaster survival and height growth on three sites in northern Greece. Forest
Ecology and Management 73, 111-115.
Ward S C, Koch J M and Ainsworth G L 1996 The effect of timing of rehabilitation
procedures on the establishment of a jarrah forest after bauxite mining. Restoration
Ecology 4, 19-24.
52
Chapter 2. Physiological and stand-level responses of jarrah (Eucalyptus
marginata) and marri (Corymbia calophylla) to seasonal drought at low-
and high-quality restored bauxite-mine sites in south-western Australia
Abstract
This study compared seasonal changes in water relations and gas exchange of jarrah
(Eucalyptus marginata) and marri (Corymbia calophylla) at adjacent 13-year-old low- and
high-quality restored bauxite-mine sites in south-western Australia. An impenetrable
subsoil at the low-quality site resulted in 61% fewer trees and 74% less standing basal area
compared with the neighbouring high-quality site. Jarrah and marri trees at the low-quality
site were 42% and 40% shorter than those at the high-quality site. Restriction of root
systems at the low-quality site significantly reduced morning stomatal conductance (gs),
photosynthesis (A), midday leaf water potential (Ψ) and average daily leaf relative water
content (RWC) in both species over the dry season. Stomatal sensitivity to drought was
high in both species; however, jarrah demonstrated a higher desiccation tolerance where Ψ
and RWC fell to -3.2 MPa and 73% compared with -2.4 MPa and 80% for marri. Given the
similarity in specific leaf area (SLA) for the two species, the lower Ψ and RWC of jarrah
combined with its higher rates of photosynthesis (A) may explain why jarrah shows faster
growth rates and is the more dominant species in restored and unmined forest stands. Marri
operated at lower gs and higher Ψ and RWC during drought which indicates that it avoided
drought to a greater extent than jarrah. Pressure-volume curves showed that cell-wall
elasticity of jarrah leaves increased in response to drought; however, they showed no
osmotic adjustment. Conversely, marri leaves had a significantly lower osmotic potential at
zero turgor in summer than in winter, indicating osmotic adjustment. Clearly, jarrah and
marri demonstrate different mechanisms for surviving drought which can potentially be
incorporated in site-species matching decisions at restored bauxite-mine sites.
Introduction
Bauxite mining is a major industry in the jarrah forest on the Darling Plateau of south-
western Australia (refer to General Introduction of a description of bauxite mining and
restoration processes, and for a description of the jarrah forest region). Post-mining
53
techniques including: direct-return of topsoil, broadcast seeding, fertiliser application and
deep-ripping of subsoil, are largely successful at rapidly establishing vegetation across the
landscape (Grant et al. 1996; Koch et al. 1996; Ward et al. 1996; Koch 2007). However,
some areas show poor growth of the two main tree species, jarrah and marri, several years
after successful establishment. Factors limiting growth at this age can include impenetrable
subsoils (Enright and Lamont 1992; Passioura 2002; Mengler et al. 2006; Kew et al. 2007;
Szota et al. 2007). Such sites have higher rates of tree mortality; however, their most
striking attribute is that the surviving trees are significantly smaller (Chapter 1). Given the
importance of stored soil moisture during the dry summer (Farrington et al. 1996), soil
depth restrictions make the possession of physiological strategies for coping with drought
essential for survival.
Jarrah and marri are co-occurring upper-canopy tree species in the northern jarrah
forest of south-western Australia (Abbott and Loneragan 1986; Abbott et al. 1989). Jarrah
is a hardy evergreen species well adapted to seasonal drought and heterogeneous soils
(Abbott et al. 1989) which is why it responds well to the post-mining landscape (Koch and
Samsa 2007). Physiological studies of jarrah at unmined sites have shown that exposure to
water stress decreases as the tree develops (Crombie et al. 1988; Crombie 1992; Stoneman
et al. 1995; Crombie 1997), presumably because root systems access an ever-increasing soil
water resource. As a mature tree in the forest, jarrah accesses water deep in the soil profile
(Farrington et al. 1996) through ancient root channels (Dell et al. 1983) which allows it to
transpire over summer while maintaining a stable water status (Doley 1967; Carbon et al.
1981; Colquhoun et al. 1984). Osmotic adjustment in jarrah has been demonstrated in the
glasshouse with seedlings exposed to high levels of water stress (Stoneman et al. 1994);
however, it has not been observed in the field (Bleby 2003; Warren et al. 2007).
In the unmined forest, marri tends to colonise areas where root development is
limited and access to soil moisture is highly variable such as shallow soils and riparian
zones susceptible to waterlogging (Harris 1956; Florence 1996). At restored bauxite mine
sites, marri tends to survive hostile sites, such as where deep-ripping has been ineffective,
to a greater extent than jarrah (J. Koch pers. comm.). Studies of marri physiology have
largely been restricted to mature forest stands as a comparison with jarrah; however, marri
is typically discussed in less detail than jarrah, presumably because it represents less of the
54
stand (typically 20-40%) and has less economic value. Jarrah maintains higher daily
transpiration rates (Grieve 1956; Carbon et al. 1981) and midday stomatal conductance
(Crombie 1992); and lower predawn (Crombie et al. 1988) and midday (Carbon et al. 1981;
Colquhoun et al. 1984; Crombie 1992) leaf water potentials over summer than marri. None
of these studies explore the reasons for these observed differences in water stress patterns
between the two species, nor do they allow us to describe their performance in response to
variable site quality.
It has been demonstrated that the physiology of larger, older trees is often markedly
different to that of smaller, younger trees (Crombie 1997; Kolb and Stone 2000; Niinemets
2002; Rust and Roloff 2002) and coppice (Crombie 1997; Wildy et al. 2004); therefore
knowledge gained from the study of mature jarrah and marri physiology may not relate to
younger stands. Furthermore, the physiology of trees at restored bauxite-mine sites may
differ from that of trees growing on undisturbed soil profiles. A further consideration is
that different species, like the dominant jarrah, or subdominant marri, may react to the new
conditions of the post-mining landscape in different ways, in particular due to soil depth,
structure and even fertility. Comparative studies of co-occurring eucalypts indicate that
they often possess different physiological mechanisms and/or access different resource
pools (Burdon and Pryor 1975; Eberbach and Burrows 2006; Grigg et al. 2008); therefore,
the fact that marri appears to maintain a higher water status over summer should be
explored, particularly in the context of introducing these species into a disturbed ecosystem
such as a restored bauxite mine.
The present study aims to assess differences in the physiological response to
drought of jarrah and marri in relation to site quality at restored bauxite mine sites, in an
attempt to identify the nature and severity of the stress (or stresses) that trees are exposed to
at low-quality restored bauxite mine sites. The study further aims to investigate whether
there are any inherent differences between jarrah and marri physiology on low- and high-
quality restored sites which would have implications for species selection and stand
management at restored bauxite mines.
55
Materials and Methods
Study site
This study was carried out in a 13-year-old restored bauxite mine pit, located approximately
10 km north-west of Dwellingup (32º43´S, 116º04´E), Western Australia, Australia. In this
study, two 1250 m2 plots (each measuring 25 m x 50 m) were established, one in a patch of
small trees, classed as ‘low-quality’, and another in an adjacent area of taller trees (‘high-
quality’) within the same restored pit. Refer to Chapter 1 for a detailed description of the
study site and the restoration process.
Weather data
The weather data presented here were recorded at the township of Dwellingup by the
Australian Bureau of Meteorology. Dwellingup has a Mediterranean-type climate with a
72-year average annual rainfall of 1258 mm, with approximately 70% falling between April
and September. The bulk of the study took place during 2004, which was a drier than
average year, with an annual rainfall of 1162 mm and annual pan evaporation of 1402 mm
(Fig. 2.1). Vapour pressure deficit (VPD) increased over the day in each month, with the
highest value recorded at 1500 hours (Australian Western Standard Time), with the
exception of the winter months where there was no increase from 1200 to 1500 hours.
Average daily VPD increased from 1.2 to 3.0 kPa in summer and from 0.1 to 0.5 kPa in
winter from 0900-1500 hours over the study period.
Stand characteristics
Initial stand characteristics were measured at both sites in May, 2003. Stand density was
determined by counting all jarrah and marri trees taller than 2 m at the two 1250 m2 plots.
Tree height was measured for all jarrah and marri trees >2 m tall at both sites, and recorded
as the height of the tallest living section of the crown. Girth over bark at breast height (1.3
m) was recorded for all stems of all jarrah and marri trees >2 m tall at both sites, and
converted to diameter over bark at breast height (DBH). Thirty pre-selected trees
representative of the size-class distribution range for each species in both stands were re-
measured in May 2005 using the same methods, in order to determine the increase in
height, DBH and BA since 2003. Six leaves per tree were collected from each of six trees
56
in August, 2004, prior to emergence of new leaves, and sealed in small zip-lock bags and
placed in an insulated box with ice packs. Leaf area was measured using a LAI-3100C (LI-
COR Inc., Lincoln, Nebraska, USA) upon returning to the laboratory, prior to oven-drying
the leaves at 70°C for 48 hours, after which their dry weights were recorded. SLA was
calculated as leaf area/ leaf dry weight.
0
50
100
150
200
250
300
350
N D J F M A M J J A S O N D J F M
Rai
nfal
l (m
m)
Eva
pora
tion
(mm
)
0
5
10
15
20
25
30
35
Tem
pera
ture
(ºC
)0
1
2
3
4
N D J F M A M J J A S O N D J F M
VP
D (k
Pa)
A
2003 2004 2005
B
0
50
100
150
200
250
300
350
N D J F M A M J J A S O N D J F M
Rai
nfal
l (m
m)
Eva
pora
tion
(mm
)
0
5
10
15
20
25
30
35
Tem
pera
ture
(ºC
)0
1
2
3
4
N D J F M A M J J A S O N D J F M
VP
D (k
Pa)
A
2003 2004 2005
B
Figure 2.1. (A) Mean monthly maximum (white circles) and minimum (grey circles) temperatures, total monthly rainfall (black bars) and total monthly pan evaporation (white bars). (B) Mean monthly vapour pressure deficit (VPD) at 0900 hours (white circles), 1200 hours (grey circles) and 1500 hours (black circles) over the study period between November, 2003 and March, 2005. All weather data were recorded by the Bureau of Meteorology at the Dwellingup weather station (32º43´S, 116º04´E), Western Australia, Australia.
Study tree selection for physiological measurements
Physiological measurements were taken on trees in the median size class for that species on
each site. At the low-quality site, jarrah trees were 4-6 m tall and marri trees were 3-6 m
57
tall. At the high-quality site, jarrah trees were 7-9 m tall while marri trees were 5-8 m tall.
Adjacent jarrah and marri were selected where possible in order to make direct
comparisons between the two species. Shaded, chlorotic and heavily predated trees were
not sampled.
Physiological measurements described below were carried out over two to three
consecutive days each month between November 2003 and April 2005. Three trees per
species were sampled at each site between 0700 and 1700 hours. Twelve new trees were
selected for measurements each month. Due to the small number of marri trees at the low-
quality site, some individuals were measured more than once during the study. Weather
conditions were often different between measurement days within any given month;
therefore measurements were taken in blocks such that direct comparisons could be made
between both sites and both species over the course of the day. If weather conditions,
particularly diurnal courses of vapour pressure deficit (VPD) were similar over the
sampling days within a month, then the data were pooled to give a single monthly figure. If
weather conditions were very different, then data from the sampling day that were most
representative of the sampling month, in meteorological terms, were used.
Leaf stomatal conductance and photosynthesis
Gas exchange was measured on sun-exposed, freshly cut branches from the upper third of
the crown. Tests were run over the year in order to determine whether measurements taken
on freshly cut sections were significantly different to those taken prior to cutting. Tests
involved measuring leaves in situ for several minutes, then cutting the branch 30-50 cm
basally and stripping the majority of leaves from the branch to reduce transpiration demand.
Response to excision was monitored for approximately 10 minutes. There was no change
in leaf functioning for at least 4-5 minutes after excision, not even in late summer, when
cutting would have the greatest effect on leaf functioning (data not shown). Only
measurements completed before this time were included in the dataset. Other studies on
jarrah have successfully used cut sections for gas-exchange measurements (Crombie 1992;
1997).
Diurnal patterns of stomatal conductance (gs), photosynthesis (A) and internal CO2
concentration (Ci) were captured each month for three trees per species, per site, with a LI-
58
6400 gas exchange system (LI-COR Inc., Lincoln, Nebraska, USA). Three mature sun-
exposed leaves were measured on each study tree. Conditions in the chamber were kept as
consistent as possible in order to compare leaf performance across seasons. Photosynthetic
photon flux density (red-blue light source) was set at 1500 μmol m-2 s-1, CO2 concentration
in the chamber ranged from 374-394 μmol mol-1 over the course of the study. Temperature
in the chamber was set at 25ºC; however, when ambient temperature was high in summer
(>35°C) the chamber temperature increased to 30-33°C.
Leaf water potential, osmotic potential and relative water content
Diurnal patterns of leaf water potential (Ψ), osmotic potential (Π) and relative water
content (RWC) were measured 4 – 6 times per day between 0700 – 1700 hours at monthly
intervals over the study period. Water potential was measured using a Scholander-type
pressure chamber (PMS Instruments, Corvallis, Oregon, USA). Three twigs bearing 3 – 4
mature sun-exposed leaves were excised from the top of the canopy on the northern side of
each of the 12 study trees (3 trees per species per site) measured each month. The sections
were measured immediately following excision. Sections were placed inside a zip-lock bag
with only the cut end protruding while inside the chamber, which was lined with wet cloth
in order to minimise evaporative losses during pressurisation (Turner 1988).
Three leaves from each of the 12 study trees (3 trees per species per site) selected
each month were placed in an airtight 5-ml cryovial (Simport, Canada) and immediately
stored on dry ice. Samples were transferred to a -20ºC freezer in the laboratory until
analysis. Samples were thawed and then crushed using a leaf press. The sap was analysed
with a Fiske 101 freezing-point depression osmometer (Fiske Associates, Model 110,
Massachusetts, USA). The osmometer was regularly calibrated with 50, 850 and 1200
mmol kg-1 standards during analysis of the samples. In order to compare osmotic
adjustment between sites and species over the course of the year, osmotic potential values
were corrected for seasonal changes in leaf relative water content.
Three sections were excised from the top of the canopy on the northern side of the
12 study trees (3 trees per species per site) selected each month. From these three sections
per tree, three mature leaves were sealed in small zip-lock bags and placed in an insulated
box with ice packs. Depending on the time of day sampled, leaves remained in the box for
59
3–10 hours prior to being weighed (fresh weight). Samples where condensation was
obvious inside the zip-lock bag were discarded. Leaves were wrapped in wet tissue paper
and stored in plastic zip-lock bags at 4°C in the dark for 12 hours to facilitate hydration.
Leaves were then blotted dry and their saturated, or turgid, weights recorded. The leaves
were then oven dried at 70ºC for 48 hours, and re-weighed to determine their dry weights.
Relative water content was calculated as: RWC = (fresh weight – dry weight) / (saturated
weight – dry weight) x 100%.
Pressure-volume curves
Pressure-volume curves were derived in March and August 2004. Sun-exposed branches
were taken from the exterior of the canopy from the northern side of five jarrah and five
marri trees at each site. Stems were immediately recut under water in 50-ml plastic vials
and leaves were wrapped in plastic film. The samples were left to hydrate overnight in the
laboratory for approximately 12 hours. The following morning the material was used to
produce pressure-volume curves. Some leaves had blotchy, dark staining which may be
due to over-saturation (Bleby 2003; Warren et al. 2007), and these leaves were not selected
for producing curves. Youngest fully expanded leaves were excised with a razor blade and
immediately weighed and transferred into a pressure bomb to determine water potential
(see above section). Leaves were placed on the laboratory bench between measurements to
facilitate dehydration. Pressure-bombing finished when water potentials of -4 to -6 MPa
were reached, and when the relationship between 1/Balancing Pressure (BP) and 1-RWC
became linear. Osmotic potential at full turgor (Π100), osmotic potential at zero turgor (Π0),
relative water content at zero turgor (RWC0) and the turgid weight to dry weight ratio were
calculated from the pressure-volume curves (Tyree and Hammel 1972; Turner 1988). Bulk
modulus of elasticity (εmax) was calculated from the slope of the relationship between
pressure potential and RWC in the positive turgor range (Turner 1988).
Data analyses
Two-way analysis of variance (ANOVA) was used to determine differences between sites
and species and the interaction site*species for the stand and tree characteristics. Two-way
ANOVA was also used to determine differences between sites and species between and
within seasons for pressure-volume curve parameters. Two-way ANOVA was used to test
60
for significant differences in gs, A, Ψ, Π and RWC between sites and species within a given
month and within a given time of day (morning, midday or afternoon). One-way ANOVA
was used to test for significant differences within site, species and time of day between
months. One-way ANOVA was also used to test for significant differences between time
of day within month, for each species at each site. Linear regression analysis was used to
determine the correlation between gs and VPD; maximum gs (gsmax) and Ψ; gsmax and RWC
and Ψ and RWC. Results are only referred to as significantly different where P<0.05. All
data were tested for normality using a Shapiro-Wilk test and log-transformations were
performed where appropriate).
Results
Stand characteristics
The low-quality site had 61% fewer trees and 74% less standing basal area than the
neighbouring high-quality site (Table 2.1). Jarrah trees represented 80% of the stand at the
low-quality site and 76% of the stand at the high-quality site. Jarrah trees constituted 88%
of the stand basal area at the low-quality site and 86% at the high-quality site. Jarrah and
marri trees at the low-quality site were 42% and 40% shorter and had 28% and 26% smaller
diameters than those at the high-quality site. The mean annual increase (2003-2005) in
height of jarrah and marri at the low-quality site was 41% and 38% less than that at the
high-quality site. There was no significant difference in the annual increase in DBH
between sites. Jarrah trees did, however, have annual increases in DBH 43% and 33%
higher than marri trees at the low-quality and high-quality sites. There was no significant
difference in SLA between sites or species.
Seasonal patterns of leaf stomatal conductance and photosynthesis
Morning gs and A were highest in late spring and declined over the dry season (December -
March) for both species at both sites, whereas midday and afternoon values peaked earlier,
at least in 2004 (Figs 2.2 and 2.3; refer to least significant difference for each time of day
for significant differences between months). Both species at both sites maintained high
stomatal conductance and rates of photosynthesis in the morning (0700–1030 hours) for the
major part of the year, with the exception of the winter months when the highest gs and A
were recorded at midday (1130–1330 hours) (Figs 2.2 and 2.3; refer to ‘†’ symbols below
61
Table 2.1. Stand and tree characteristics at low-quality and high-quality restored bauxite mine sites containing jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) (mean standard error in parentheses with n = 168, 407, 42 and 126 for low-quality jarrah, high-quality jarrah, low-quality marri and high-quality marri). Mean annual growth rates (2003-2005) for height and diameter over bark at breast height (DBH) are also presented with mean standard error in parentheses (n=30 trees per site, per species). Specific leaf area (SLA) was measured in August, 2004 (n=36 leaves per site, per species). All P-values are derived from two-way ANOVA. P Site and P Species represent the P-values for differences between sites and species, and P Site*P Species represents the interaction site*species. Within rows, different letters indicate significant differences between site and species (using the maximum least significant difference from the interaction site*species). N.S refers to no significant difference (P> 0.05).
Low-quality High-quality Low-quality High-quality
jarrah jarrah marri marri P Site P Species P Site*P Species
Stand density (trees ha-1) 1344 3256 336 1008
Stand basal area (m2 ha-1) 11.4 43.4 1.5 6.8
Tree height (m) 4.6 (±0.1)b 8.0 (±0.1)d 3.9 (±0.3)a 6.5 (±0.2)c <0.001 <0.001 0.01
Tree DBH (cm) 8.4 (±0.3)b 11.6 (±0.2)c 5.9 (±0.5)a 8.0 (±0.3)b <0.001 <0.001 0.01
Height growth rate (m year-1) 0.43 (±0.03)b 0.73 (±0.04)c 0.26 (±0.02)a 0.42 (±0.02)b <0.001 <0.001 0.04
DBH growth rate (cm year-1) 0.60 (±0.04)b 0.57 (±0.01)b 0.42 (±0.03)a 0.43 (±0.04)a n.s. <0.001 0.05
SLA (cm2 g-1) 57.0 (±0.9) 55.3 (±0.8) 57.1 (±1.2) 59.2 (±0.9) n.s n.s. n.s.
62
bottom x-axis for significant differences between time of day for each species at each site).
Both species at both sites showed decreasing gs and A over the course of the day during the
dry season (Figs 2.2 and 2.3). Jarrah and marri at the low-quality site showed lower
morning gs and A over the dry season than at the high-quality site (Figs 2.2A, 2.2B, 2.3A
and 2.3B; refer to ‘*’ symbols for each time of day for significant differences for the
interaction site*species within each month). Jarrah at the low-quality site showed higher
midday and afternoon gs over spring and early summer than at the high-quality site (Figs
2.2C and 2.2E). Jarrah maintained higher gs and A over the course of the year than marri
did at both sites, except late in the dry season when they were similar (Figs 2.2 and 2.3).
Seasonal patterns of leaf water potential, osmotic potential and relative water content
Jarrah and marri at both sites showed their highest midday Ψ in winter and their lowest in
summer (Figs 2.4A and 2.4B). Jarrah at the low-quality site maintained higher Ψ over
spring and early summer, and lower Ψ over mid to late summer than it did at the high-
quality site (Fig. 2.4A). There was no significant difference in Ψ between sites over the dry
season for marri (Fig. 2.4B). Jarrah maintained significantly lower Ψ over the dry season
than marri did at both sites (Figs 2.4A and 2.4B).
Seasonal variation in Π was similar to that for Ψ, with highest values in winter and
lower values in summer (Figs 2.4C and 2.4D). Jarrah showed no consistent seasonal
difference between sites during the year; however, marri had lower Π at the low-quality site
compared with that at the high-quality site over the dry season.
There was no significant diurnal trend in leaf relative water content on any of the
measurement days over the course of the study (data not shown). Consequently, all relative
water content results are expressed as averages for the measurement day(s) within a given
month. Jarrah and marri at both sites had their highest RWCs in winter and their lowest
late in the dry season (Figs 2.4E and 2.4F). Jarrah leaves at the low-quality site dried out to
a greater extent (73% RWC) than marri leaves did (80% RWC) in late summer (Figs 2.4E
and 2.4F).
63
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F M
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F M
gs (m
mol
m-2
s-1
)Morning
Midday
2003 2004 2005 2003 2004 2005
Afternoon
JARRAH MARRI
Morning
Midday
Afternoon
A
C
E
B
D
F
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
* * * * ** ** * * * * * ** * * * ** ** * * * * * *
* * * * ** *** * * * * * * ** *** * *
* * * * * * * * *
LQ
HQ
† † † † ††
† † † † † † † † † † †† † † † †† † † † † † † † † † † † † † † † †† † † † †† † † †
* * * * * * * * *
†
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F MMonth
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F M
gs (m
mol
m-2
s-1
)
0
100
200
300
400
500
600
N D J F M A M J J A S O N D J F M
gs (m
mol
m-2
s-1
)Morning
Midday
2003 2004 2005 2003 2004 2005
Afternoon
JARRAH MARRI
Morning
Midday
Afternoon
A
C
E
B
D
F
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
* * * * ** ** * * * * * ** * * * ** ** * * * * * *
* * * * ** *** * * * * * * ** *** * *
* * * * * * * * *
LQ
HQ
† † † † ††
† † † † † † † † † † †† † † † †† † † † † † † † † † † † † † † † †† † † † †† † † †
* * * * * * * * *
† Figure 2.2. Morning (A and B), midday (C and D) and afternoon (E and F) stomatal conductance (gs) of jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) at low-quality (black) and high-quality (white) restored mine sites. Morning measurements were taken between 0700 and 1030 hours, midday measurements were taken between 1130 and 1330 hours, and afternoon measurements were taken between 1400 and 1700 hours. Measurements were taken on a monthly basis between November, 2003 and March, 2005. Each point represents an average value of three trees, sampled between 1-3 times within each time period. Bars on mean values represent mean standard error (n=3-9). Bold bars represent least significant difference (P<0.05) between months within site and species for the low-quality (LQ) and high-quality (HQ) sites. Significant differences (P<0.05) for the interaction site*species within any given month are represented by an asterisk. Significant differences (P<0.05) between time of day within site and species are represented by † below the bottom x-axis of the figure.
64
0
5
10
15
20
N D J F M A M J J A S O N D J F M
A (μ
mol
m-2
s-1
)
0
5
10
15
20
N D J F M A M J J A S O N D J F M
A (μ
mol
m-2
s-1
)
0
5
10
15
20
N D J F M A M J J A S O N D J F M
A (μ
mol
m-2
s-1
)
0
5
10
15
20
N D J F M A M J J A S O N D J F M
A (μ
mol
m-2
s-1
)
0
5
10
15
20
N D J F M A M J J A S O N D J F M
A (μ
mol
m-2
s-1
)
0
5
10
15
20
N D J F M A M J J A S O N D J F M
A (μ
mol
m-2
s-1
)Morning
Midday
2003 2004 2005 2003 2004 2005
Afternoon
JARRAH MARRI
Morning
Midday
Afternoon
A
C
E
B
D
F
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
* * ** ** * *
* * * * ** *** *
LQ
HQ
† † † † † † † † † † † †† † †† † † † †† † † † † † † † † † † † † † † † †† † † † †† †
LQ HQ
* * * * * * * ** *** * * * *
* * * * * ** ** * * * * *
*** * * ** * ** * ** * **
*
† ††
† † †† † †
Figure 2.3. Morning (A and B), midday (C and D) and afternoon (E and F) photosynthesis (A) of jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) at low-quality (black) and high-quality (white) restored bauxite mine sites. Morning measurements were taken between 0700 and 1030 hours, midday measurements were taken between 1130 and 1330 hours, and afternoon measurements were taken between 1400 and 1700 hours. Measurements were taken on a monthly basis between November, 2003 and March, 2005. Each point represents an average value of three trees, sampled between 1-3 times within each time period. Bars on mean values represent mean standard error (n=3-9). Bold bars represent least significant difference (P<0.05) between months within site and species for the low-quality (LQ) and high-quality (HQ) sites. Significant differences (P<0.05) for the interaction site*species within any given month are represented by an asterisk. Significant differences (P<0.05) between time of day within site and species are represented by † below the bottom x-axis of the figure.
65
70
80
90
100
N D J F M A M J J A S O N D J F M A
RW
C (%
)
70
80
90
100
N D J F M A M J J A S O N D J F M A
RW
C (%
)
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Month
Π (M
Pa)
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Month
П (M
Pa)
-4
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Month
ψ (M
Pa)
-4
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Monthψ
(MP
a)
2003 2004 2005 2003 2004 2005
E F
A
C
B
D
JARRAH MARRI
* * * * * * * * * * * *
* * * * * * * * * * *
* * * * * * * * * * * * * * * * * * * * * * * * * * * *
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
*
70
80
90
100
N D J F M A M J J A S O N D J F M A
RW
C (%
)
70
80
90
100
N D J F M A M J J A S O N D J F M A
RW
C (%
)
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Month
Π (M
Pa)
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Month
П (M
Pa)
-4
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Month
ψ (M
Pa)
-4
-3
-2
-1
0N D J F M A M J J A S O N D J F M A
Monthψ
(MP
a)
2003 2004 2005 2003 2004 2005
E F
A
C
B
D
JARRAH MARRI
* * * * * * * * * * * *
* * * * * * * * * * *
* * * * * * * * * * * * * * * * * * * * * * * * * * * *
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
LQ HQ
*
Figure 2.4. Midday leaf water potential (Ψ) (A and B), daily average osmotic potential (Π) corrected for relative water content (C and D) and daily average relative water content (RWC) (E and F) of jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) at low-quality (black) and high-quality (white) restored bauxite mine sites. Midday leaf water potential values were captured between 1130 and 1330 hours and are the average of one shoot from each of three trees. The number of sampling periods over the midday block varied between one and three over the course of the study. Daily average values for Π and RWC are the average of three leaves from three trees for each sampling time over the day. Number of sampling times over the day varied between three and six over the course of the study as determined by day length and weather conditions. All water relations measurements were taken on a monthly basis between November, 2003 and April, 2005. Bars on mean values represent mean standard error (n=3-18). Bold bars represent least significant difference (P<0.05) between months within site and species for the low-quality (LQ) and high-quality (HQ) sites. Significant differences (P<0.05) for the interaction site*species within any given month are represented by an asterisk.
66
Stomatal sensitivity in relation to vapour pressure deficit, leaf water potential and relative
water content
During winter and spring, jarrah and marri at both sites maintained high gs over the course
of the day as VPD increased (Figs 2.5A and 2.5B). In mid-summer, however leaves of both
species showed a significant decrease in gs over the day as VPD increased, with jarrah and
marri at the low-quality site maintaining lower gs for any given VPD (Figs 2.5C and 2.5D).
Conductance was low for both species at both the low- and high-quality sites in late
summer/autumn at the start of the day and declined further over the day in response to
increasing VPD, even though the maximum VPD on the measurement days was lower than
that recorded during winter/spring and early summer (Figs 2.5E and 2.5F).
For jarrah, the highest daily value for gs (typically recorded in the morning)
decreased linearly with midday water potential, whereas there was no correlation between
morning gs and Ψ for marri (Figs 2.6A and 2.6B). Leaves of both species, however,
showed a similar linear decrease of morning gs with RWC (Figs 2.6C and 2.6D).
Pressure-volume analysis
There was no significant difference in Π100, RWC0 or TW:DW between sites, between
species or between seasons. Values for Π0 of jarrah did not differ between winter and
summer at either site; however, Π0 was significantly lower (P<0.02) for marri leaves
analysed in summer compared with those in winter at both sites (Table 2.2). There was no
significant difference in Π0 between jarrah and marri in winter at either site; however,
jarrah had significantly higher Π0 (P<0.02) than marri in summer at both sites. Jarrah
leaves analysed in winter had significantly higher bulk modulus of elasticity, εmax,
(P<0.001) than those analysed in summer at both sites. Elasticity did not differ between
winter and summer for marri at either site. Jarrah at both sites had significantly higher εmax
(P<0.001) than marri in winter; however, there was no significant difference between jarrah
and marri in summer at either site.
67
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs = 282.8 - 17.9VPD, r2 = 0.13
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs (m
mol
m-2
s-1
) gs = 346.1 - 14.0VPD, r2 = 0.05BA
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs = 328.0 - 53.7VPD, r2 = 0.50
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs (m
mol
m-2
s-1
) gs = 465.6 - 88.7VPD, r2 = 0.64
0
100
200
300
400
500
600
0 1 2 3 4 5 6VPD (kPa)
gs = 256.1 - 62.3VPD, r2 = 0.46
0
100
200
300
400
500
600
0 1 2 3 4 5 6VPD (kPa)
gs (m
mol
m-2
s-1
) gs = 201.4 - 50.5VPD, r2 = 0.43
C D
E F
JARRAH MARRI
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs = 282.8 - 17.9VPD, r2 = 0.13
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs (m
mol
m-2
s-1
) gs = 346.1 - 14.0VPD, r2 = 0.05BA
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs = 328.0 - 53.7VPD, r2 = 0.50
0
100
200
300
400
500
600
0 1 2 3 4 5 6
gs (m
mol
m-2
s-1
) gs = 465.6 - 88.7VPD, r2 = 0.64
0
100
200
300
400
500
600
0 1 2 3 4 5 6VPD (kPa)
gs = 256.1 - 62.3VPD, r2 = 0.46
0
100
200
300
400
500
600
0 1 2 3 4 5 6VPD (kPa)
gs (m
mol
m-2
s-1
) gs = 201.4 - 50.5VPD, r2 = 0.43
C D
E F
JARRAH MARRI
Figure 2.5. Morning (white), midday (grey) and afternoon (black) stomatal conductance (gs) in relation to Vapour Pressure Deficit (VPD) during ‘winter/spring’ (June – December; A and B), ‘mid-summer’ (January – February; C and D) and ‘late summer/autumn’ (March – May; E and F) for jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) at low-quality and high-quality restored bauxite mine sites. Morning values were taken between 0700 and 1030 hours, midday measurements were taken between 1130 and 1330 hours and afternoon measurements were taken between 1400 and 1700 hours. Measurements were taken on a monthly basis between November, 2003 and March, 2005. Each point represents an average value of three trees, sampled between 1-3 times within each time period. Bars represent mean standard error (n=3-9).
68
0
100
200
300
400
500
600
70 80 90 100RWC (%)
gs (m
mol
m-2
s-1
)
gs= 26.5RWC - 1956.1, r2 = 0.510
100
200
300
400
500
600
70 80 90 100RWC (%)
gs (m
mol
m-2
s-1
)
gs= 25.6RWC - 1737.2, r2 = 0.64
0
100
200
300
400
500
600
-4 -3 -2 -1 0Ψ (MPa)
gs (m
mol
m-2
s-1
)
gs= 66.9ψ + 409.0, r2 = 0.070
100
200
300
400
500
600
-4 -3 -2 -1 0Ψ (MPa)
gs (m
mol
m-2
s-1
)
gs= 276.5ψ + 1031.9, r2 = 0.56
BA
DC
JARRAH MARRI
0
100
200
300
400
500
600
70 80 90 100RWC (%)
gs (m
mol
m-2
s-1
)
gs= 26.5RWC - 1956.1, r2 = 0.510
100
200
300
400
500
600
70 80 90 100RWC (%)
gs (m
mol
m-2
s-1
)
gs= 25.6RWC - 1737.2, r2 = 0.64
0
100
200
300
400
500
600
-4 -3 -2 -1 0Ψ (MPa)
gs (m
mol
m-2
s-1
)
gs= 66.9ψ + 409.0, r2 = 0.070
100
200
300
400
500
600
-4 -3 -2 -1 0Ψ (MPa)
gs (m
mol
m-2
s-1
)
gs= 276.5ψ + 1031.9, r2 = 0.56
BA
DC
JARRAH MARRI
Figure 2.6. Relationship between morning stomatal conductance (gs) and midday water potential (Ψ; A and B), and average daily relative water content (RWC; C and D) for Eucalyptus marginata (jarrah) and Corymbia calophylla (marri) from both low-quality (black) and high-quality (white) restored bauxite mine sites. Morning stomatal conductance measurements were taken between 0700 and 1030 hours and are the average 1-3 leaves per tree from three trees. Average daily RWC measurements are the average of three leaves collected from three trees sampled at 3-6 times over the day. Each point represents data captured for each month between November, 2003 and March, 2005. Data for April-September, 2004, are omitted to avoid the complication of low gs as a result of low morning Vapour Pressure Deficits (VPD < 1 kPa) and/or temperature (< 15ºC). Bars represent mean standard error (n=3-18).
69
Table 2.2. Parameters derived from pressure-volume curves including osmotic potential at full (П100) and zero (П0) turgor, bulk modulus of elasticity (εmax), relative water content at zero turgor (RWC0) and the ratio of turgid weight to dry weight (TW:DW) for jarrah (Eucalyptus marginata) and marri (Corymbia calophylla) at low- and high-quality restored bauxite mine sites. Values represent the mean for each parameter (mean standard error presented in parentheses; n=5) of five leaves per site, per species, per season. All P-values are derived from two-way ANOVA. P Species and P Season represent the P-values for differences between species within season and differences between seasons within species. Site differences were not significant. The interaction site*species and site*season were not significant either. Different lower-case letters indicate significant differences between species within season (P=P Species) and different upper-case letters indicate significant differences between seasons within species (P=P Season). N.s. refers to no significant difference (P> 0.05).
Π100 (MPa) Π0 (MPa) εmax (MPa) RWC0 (%) TW:DW jarrah marri jarrah marri jarrah marri jarrah marri jarrah marri Winter Low-quality -2.0
(±0.1) -1.7
(±0.2) -2.4
(±0.0) A -2.2 (±0.2)
B 23.5 b (±1.9)
6.9 a (±1.2)
88.8 (±1.1)
86.4 (±1.7)
2.19 (±0.04)
2.24 (±0.05)
High-quality -2.0 (±0.1)
-1.8 (±0.3)
-2.3 (±0.1)
A -2.1 (±0.3)
B 24.2 b (±2.9)
8.0 a (±2.3)
89.2 (±1.7)
87.1 (±1.5)
2.21 (±0.05)
2.35 (±0.02)
P Species n.s. n.s. <0.001 n.s. n.s. Summer Low-quality -1.9
(±0.1) -2.0
(±0.1) -2.0 a
(±0.1) B -2.8 b (±0.1)
A 8.5 b (±1.0)
6.0 a (±1.3)
83.1 (±1.5)
86.7 (±2.1)
2.38 (±0.07)
2.26 (±0.07)
High-quality -1.8 (±0.1)
-1.9 (±0.2)
-2.2 a (±0.0)
B -2.7 b (±0.0)
A 8.5 b (±0.1)
4.7 a (±0.6)
84.8 (±1.8)
86.9 (±2.9)
2.09 (±0.01)
2.24 (±0.16)
P Species n.s. 0.01 0.04 n.s. n.s. P Season n.s. n.s. n.s. 0.03 <0.001 n.s. n.s. n.s. n.s. n.s.
70
Discussion
Key physiological differences between low- and high-quality restored sites
The results show clear physiological differences between low- and high-quality restored
bauxite mine sites. Plant water status and physiological functioning were substantially
reduced at the low-quality site, compared with the high-quality site, during summer for
both jarrah and marri, indicating that soil moisture availability was lower at the low-quality
site. The severity of water stress at the low-quality site was substantially greater than
previously reported for jarrah (-3.2 MPa), despite being recorded in a high-rainfall zone
location (1258 mm yr-1). In the first substantial study of the physiological response of
jarrah to drought at restored bauxite mine sites, Bleby (2003) showed that 6-9-year-old
saplings at a low-rainfall (~600 mm yr-1) site maintained similar minimum water potentials
(-2.5 MPa) to those at a high-rainfall (~1200 mm yr-1) site (-2.7 MPa); despite obvious
differences in available soil moisture. In unmined forest, jarrah saplings at low-rainfall
(630-750 mm yr-1) sites recorded similar minimum Ψ to those at high-rainfall (1250-1350
mm yr-1) sites (-2.35 and -2.46 MPa); while mature trees often recorded much higher Ψ (-
1.40 to -2.03 MPa) at high-rainfall sites compared with low-rainfall sites (-2.29 to -2.95
MPa) (Colquhoun et al. 1984; Crombie 1992; 1997).
Lower site water availability is very likely due to limited access of roots to soil
moisture. Water is predominantly found in kaolinitic clay soils beneath the mottled bauxite
deposit prior to mining (Carbon et al. 1980), and within the top metre of the soil profile at
restored bauxite mine sites (Koch 2007). Excavations and descriptions of root-system
morphology at these sites (Szota et al. 2007; Chapter 1) revealed that the high-quality site
had a kaolinitic clay subsoil that was easily accessed by coarse roots (>5 mm in diameter)
through riplines, while coarse roots at the low-quality site were restricted to sandy/gravel
material in the top 0.5 m of the soil profile by an impenetrable cemented quartz layer (Kew
et al. 2007). Higher water stress at the low-quality site was the most likely cause of the
comparatively low stand density and slow tree growth rates. A range of previous studies
have shown that plants with restricted root systems caused by mining-related earthworks
are more susceptible to water stress and less productive (Enright and Lamont 1992;
Varelides and Kritikos 1995; Ashby 1997; Rokich et al. 2001).
71
Although water content of soils at depth was not measured in this study, previous
studies in the jarrah forest have demonstrated that soil water stores at depth are at their
maximum from August to November (Farrington et al. 1996). Over this period in the
present study, jarrah maintained similar morning gs at both sites; however, gs declined over
the day for jarrah at the high-quality site, but not at the low-quality site. Jarrah midday Ψ
values were also lower at the high-quality site over the same period; however, there was no
difference between sites in RWC. These results suggest that the higher stand density and
growth rates at the high-quality site increased competition for water over the period of leaf
expansion (Abbott et al. 1989) which indicates that tree density at the high-quality site
(4264 stems ha-1) was too high and that increased competition for water in maturing stands
may suppress growth. Grant et al. (2007) recommended that restored sites with high
stocking densities should be thinned to decrease tree water use and increase growth of
retained stems. The results presented here support this recommendation on the basis that
thinning is likely to decrease competition between trees. Current tree density targets of
1300 stems ha-1 at age nine months (Grant 2006) are unlikely to cause such high levels of
competition for water resources at restored bauxite-mine sites.
The fact that trees at the low-quality site were able to achieve similar rates of A and
gs as those at the high-quality site under favourable conditions (high soil moisture and
moderate-high VPD) suggests no inherent limitation in the maximum rate at which the
hydraulic system of the trees can supply water to the leaves. In a summer irrigation
experiment at low- (~600 mm yr-1) and high-rainfall (~1200 mm yr-1) sites, Bleby (2003)
showed that saplings at the high-rainfall site increased gs, while those at the low-rainfall
site did not. This result was explained by the hypothesis that saplings at the low-rainfall
site had a lower hydraulic conductivity, such that transpiration and stomatal conductance
were low, even when water supply was not limiting (Bleby 2003). Seasonal data, however,
showed that saplings at the low-rainfall site were able to achieve similar ‘maximum’ gs in
spring/early summer as those at the high-rainfall site (Bleby 2003); therefore an alternative
interpretation of this data is that gs was being limited by a different factor than water
availability at the low-rainfall site, such as high temperature, VPD and/or irradiance, or by
an alternative mechanism such as release of abscisic acid (ABA) from the roots (Davies et
al. 1990; Davies and Zhang 1991).
72
Key physiological differences between species in response to site conditions
In the present study, jarrah and marri differed substantially in their water status and
physiological functioning during drought. Jarrah maintained higher gs and A than marri for
the majority of the year, especially over the dry season; a result that has also been recorded
for mature jarrah and marri in unmined forest (Crombie 1992). This result was not
expected as marri leaves are anatomically suited to having a higher photosynthetic capacity
than jarrah leaves, in that the leaves of marri are thicker, have a higher proportion of
mesophyll and a higher stomatal density per unit leaf area (Ridge et al. 1984). Growth
rates are typically poorly correlated with photosynthetic rates and generally positively
correlated with SLA (Lambers and Poorter 1992). However, in the absence of differences
in SLA between the two species, higher photosynthetic rates over the year may contribute
to the faster growth rates observed for jarrah compared with marri.
Jarrah operated at higher gs and A at lower Ψ compared with marri. A number of
studies have shown that jarrah maintains lower Ψ than marri across a range of ages and size
classes at both mined and unmined sites (Carbon et al. 1981; Colquhoun et al. 1984;
Crombie et al. 1988; Crombie 1992); however, this difference has never been discussed in
detail. Over the dry season in the present study, RWC fell to 73% for jarrah and 80% for
marri which indicates that jarrah has a higher desiccation tolerance (Pook et al. 1966;
Davidson and Reid 1989; Gulías et al. 2002) than marri. Maintenance of a lower Ψ may
give jarrah a greater ability to access soil moisture during drought compared with marri,
which may be a contributing factor to its dominance in the forest. Superior exploitation of
soil water resources can allow dominant Eucalyptus species to out-compete subdominants
during drought (Eberbach and Burrows 2006). Superior access to soil water resources is
unlikely in the present study, particularly at the low-quality site where all coarse roots were
restricted to the top 0.5 m of the soil profile (Szota et al. 2007). The fact that marri leaves
operate at lower gs and higher Ψ and RWC under the same conditions in the field indicates
that marri uses water more conservatively than jarrah and therefore has an enhanced ability
to survive extended periods of drought.
Maintenance of higher water potentials during drought is often explained by higher
stomatal sensitivity, primarily in response to high VPD and/or declining soil water status.
In the present study, stomata of jarrah and marri were insensitive to increasing VPD over
73
the day when soil water availability was at its maximum in spring/early summer
(Farrington et al. 1996). As Ψ declined over summer, gs decreased in response to
increasing VPD over the day, indicating that stomata remained responsive to VPD;
however, gs was primarily governed by leaf water status (Mott and Parkhurst 1991; Sasse
and Sands 1996; Bhaskar and Ackerly 2006; Flexas et al. 2006) in jarrah and marri. This is
a common trend in eucalypts from seasonally dry environments (Doley 1967; Carbon et al.
1981; Pereira et al. 1986; Davidson and Reid 1989; Fordyce et al. 1997; Prior et al. 1997;
Faria et al. 1998; Thomas and Eamus 1999; MacFarlane et al. 2004). Stomatal
conductance was lowest in late summer/autumn when VPD was lower than in mid-summer
and water status was lowest (lowest Ψ and RWC) which indicates that by this time gs was
limited by low water availability at both sites and for both species. Although conductance
was at its lowest late in the dry season, high gs was still achieved in the morning, indicating
that gs remained sensitive to diurnal variation in VPD; however, it was much less sensitive
than in mid-summer. Bleby (2003) showed in 6-9 year old jarrah saplings at restored
bauxite mines that transpiration (E) was positively correlated with VPD to a point,
presumably a soil-moisture threshold, after which E ‘decoupled’ from VPD and declined
linearly, irrespective of further changes in VPD. This response has also been demonstrated
for jarrah in the glasshouse (Stoneman et al. 1994) and in the field with 1-2 year old
seedlings (Stoneman et al. 1995) and in mature forest (Doley 1967; Crombie 1992). The
declining morning gs late in the dry season coupled with stomatal closure earlier in the day
at relatively low VPDs in the present study agrees with the observed linear decrease in E
shown by Bleby (2003).
Stomatal sensitivity has previously been described by correlating stomatal
conductance with water potential (Pereira et al. 1987; White et al. 2000; Brodribb and
Holbrook 2003; Franks et al. 2007) or relative water content (Gulías et al. 2002). In the
present study, the slope of the relationship between gs and Ψ for jarrah was similar to that
of Eucalyptus camaldulensis Dehnhardt, which White et al. (2000) considered to have
stomata highly sensitive to changes in Ψ. Bleby (2003) showed that gs increased as Ψ
increased in drought-exposed jarrah saplings at both mined and unmined sites, which also
indicates a high stomatal sensitivity to declining plant water status. This high stomatal
sensitivity did not stop the development of low water potentials, which was also reported
74
by Warren et al. (2007) for 7-year-old jarrah; and by Franks et al. (2007) for E.
gomphocephala from the coastal plain of south-western Australia. In the present study, the
correlation between gs and Ψ was poor for marri, which suggests that marri potentially has
a low stomatal sensitivity to declining plant water status and may indicate the presence of
an alternative mechanism for stomatal regulation, such as release of ABA from roots
(Davies et al. 1990). The slope of morning gs and RWC, however, was similar for jarrah
and marri, indicating that their stomata were equally sensitive to decreases in RWC, despite
the fact that the RWC of jarrah was 7% lower than that of marri at the peak of the dry
season. High stomatal sensitivity is a trait typical of eucalypts from environments with
high water availability. For example, at a low-rainfall (480 mm yr-1) site, White et al.
(2000) found that two low-rainfall zone species (E. leucoxylon F. Muell. and E. platypus
subsp. platypus Hook.) had lower stomatal sensitivities to declining leaf water status than
the riparian E. camaldulensis. E. pauciflora Sieb. ex Spreng. from the Snowy Mountains of
New South Wales (Körner and Cochrane 1985), Eucalyptus grandis Hill ex Maiden (Fan et
al. 1994) and E. cloeziana F. Muell. (Ngugi et al. 2003) from the moist subtropics of
southern Queensland and E. regnans F. Muell. (Ashton and Sandiford 1988) and E. nitens
(Deane & Maiden) Maiden (White et al. 1996) from high-rainfall mountain ranges in
Victoria all demonstrate strong stomatal sensitivity to leaf water deficits.
Stomatal sensitivity to leaf water potential is influenced by leaf cell-wall elasticity
(White et al. 2000; Carter et al. 2006). Leaves with high cell-wall elasticity can effectively
maintain turgor as leaf water content declines, because the concentration of their solutes
increases as a consequence of the reduced cell volume (Zimmermann and Steudle 1978).
In the present study, jarrah leaves had rigid cell walls in winter (high εmax); however, their
elasticity increased (εmax decreased) in response to drought, suggesting an enhanced ability
to maintain turgor at low RWC and Ψ during drought (White et al. 2000). This finding has
not been presented for jarrah previously and does not agree with that of Stoneman et al.
(1994) who showed that jarrah seedlings subjected to drought in the glasshouse showed no
change in cell-wall elasticity. Marri leaves in the present study were highly elastic at both
measurement times. High cell-wall elasticity tends to be a feature of drought-tolerant rather
than drought-avoiding eucalypts (Clayton-Greene 1983; Prior and Eamus 1999; White et al.
2000). It must be noted that leaf age has a bearing on comparisons between summer and
75
winter (Prior and Eamus 1999); however, the similar TW:DW between seasons for both
species indicates that the leaves used were not significantly different in structure. Abbott et
al. (1989) describes jarrah as producing new leaves from naked buds in late winter which
expand until early summer, then mature and harden over the summer months; thus it is
unlikely that major structural leaf changes took place between March and August when
pressure-volume curves were derived.
Elastic adjustment may explain how jarrah was able to tolerate lower Ψ and RWC
over the dry season; however, it does not explain how marri was able to maintain a higher
water status than jarrah at both sites. Pressure-volume curves showed that elastic
adjustments in jarrah were not accompanied by accumulation of solutes which is consistent
with previous studies on jarrah saplings in the field (Crombie 1997; Bleby 2003; Warren et
al. 2007), but not with studies on seedlings subjected to high water deficits in the
glasshouse (Stoneman et al. 1994). The relatively rapid onset and high severity of the
drought stress applied to seedlings in the glasshouse by Stoneman et al. (1994) may explain
why osmotic adjustment has not been observed in the field. In contrast to jarrah, marri
leaves had a significantly lower Π0 in summer than in winter, indicating osmotic
adjustment. Marri leaves had similarly elastic cell walls in winter and summer; therefore
the higher Π0 in summer was unlikely to be due to an increase in cell-wall elasticity. The
magnitude of osmotic adjustment in marri was similar to levels recorded for most eucalypts
exposed to seasonal drought, including E. tetrodonta (Prior and Eamus 1999), E. behriana,
E. microcarpa (Clayton-Greene 1983) and E. nitens (White et al. 1996). Seasonal patterns
in Π confirmed that marri showed lower osmotic potentials than jarrah during drought. The
combination of a low εmax and active accumulation of solutes may contribute to turgor
maintenance as leaf RWC declines in marri, and therefore make it better able to survive
periods of low water availability than jarrah. This potential advantage of marri is not
supported by a higher productivity; however, ability to survive drought and tree size are
rarely positively correlated in eucalypts (Merchant et al. 2006). The present study is the
first evidence of osmotic adjustment in marri. Many eucalypts from contrasting
environments exhibit osmotic adjustment in response to drought (Clayton-Greene 1983;
Tuomela 1997; Li 1998; White et al. 2000; Merchant et al. 2007; Arndt et al. 2008).
76
Conclusions
The present findings show that seasonal physiology of jarrah and marri is heavily
influenced by site quality and that mechanisms for drought-tolerance are enhanced under
adverse soil conditions. Jarrah leaves achieve higher gs and A at lower Ψ and RWC during
drought, which may explain why jarrah is dominant relative to marri, both in unmined
mature forest and restored mine sites. Marri leaves had lower gs and A at higher Ψ and
RWC over the dry season when compared with jarrah, indicating that they operate more
conservatively during drought. This ability may be linked to the ability of marri leaves to
osmotically adjust, rather than being due to a higher stomatal sensitivity to VPD, and is
potentially linked to other unexplored triggers such as release of ABA from roots. With
regard to the implications of this study for mine-site restoration, it is clear that both jarrah
and marri are able to tolerate drought-prone sites. However, this study suggests that the
more conservative physiological functioning of marri potentially improves its ability to
survive low-quality sites with low soil-moisture-storage capacity.
References
Abbott I, Dell B and Loneragan O 1989 The jarrah plant. In The jarrah forest: a complex
Mediterranean ecosystem. Eds. B Dell, J J Havel and N Malajczuk. pp 41-51.
Kluwer Academic Publishers, Dordrecht.
Abbott I and Loneragan O 1986 Ecology of jarrah (Eucalyptus marginata) in the Northern
Jarrah Forest of Western Australia. p. 137. Department of Conservation and Land
Management, Perth.
Arndt S K, Livesley S J, Merchant A, Bleby T M and Grierson P F 2008 Quercitol and
osmotic adaptation of field-grown Eucalyptus under seasonal drought stress. Plant,
Cell and Environment 31, 915-924.
Ashby W C 1997 Soil ripping and herbicides enhance tree and shrub restoration on
stripmines. Restoration Ecology 5, 169-177.
Ashton D H and Sandiford E M 1988 Natural hybridisation between Eucalyptus regnans F.
Muell. and E. macroryncha F. Muell. in the cathedral range, Victoria. Australian
Journal of Botany 36, 1-22.
77
Bhaskar R and Ackerly D D 2006 Ecological relevance of minimum seasonal water
potentials. Physiologia Plantarum 127, 353-359.
Bleby T M 2003 Water use, ecophysiology and hydraulic architecture of Eucalyptus
marginata (jarrah) growing on mine rehabilitation sites in the jarrah forest of south-
western Australia. In School of Plant Biology. p. 262. The University of Western
Australia, Perth.
Brodribb T J and Holbrook N M 2003 Stomatal closure during leaf dehydration, correlation
with other leaf physiological traits. Plant Physiology 132, 2166-2173.
Burdon J J and Pryor J D 1975 Interspecific competition between eucalypt seedlings.
Australian Journal of Botany 23, 225-229.
Carbon B A, Bartle G A and Murray A M 1981 Patterns of water stress and transpiration in
jarrah (Eucalyptus marginata Don. ex Sm.) forests. Australian Forest Research 11,
191-200.
Carbon B A, Bartle G A, Murray A M and Macpherson D K 1980 The distribution of root
length, and the limits to flow of soil water to roots in a dry sclerophyll forest. Forest
Science 26, 656-664.
Carter J L, Veneklaas E J, Colmer T D, Eastham J and Hatton T J 2006 Contrasting water
relations of three coastal tree species with different exposure to salinity. Physiologia
Plantarum 127, 360-373.
Clayton-Greene K A 1983 The tissue water relationships of Callitris columellaris,
Eucalyptus melliodora and Eucalyptus microcarpa investigated using the pressure-
volume technique. Oecologia 57, 368-373.
Colquhoun I J, Ridge R W, Bell D T, Loneragan W A and Kuo J 1984 Comparative studies
in selected species of Eucalyptus used in rehabilitation of the northern jarrah forest,
Western Australia. I. Patterns of xylem pressure potential and diffusive resistance of
leaves. Australian Journal of Botany 32, 367-373.
Crombie D S 1992 Root depth, leaf area and daytime water relations of jarrah (Eucalyptus
marginata) forest overstorey and understorey during summer drought. Australian
Journal of Botany 40, 113-122.
78
Crombie D S 1997 Water relations of jarrah (Eucalyptus marginata) regeneration from the
seedling to the mature tree and of stump coppice. Forest Ecology and Management.
97, 293-303.
Crombie D S, Tippett J T and Hill T C 1988 Dawn water potential and root depth of trees
and understorey species in south-western Australia. Australian Journal of Botany
36, 621-631.
Davidson N J and Reid J B 1989 Response of eucalypt species to drought. Australian
Journal of Ecology 14, 139-156.
Davies W J, Mansfield T A and Hetherington A M 1990 Sensing of soil water status and
the regulation of plant growth and development. Plant, Cell and Environment 13,
709-719.
Davies W J and Zhang J 1991 Root signals and the regulation of growth and development
of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular
Biology 42, 55-76.
Dell B, Bartle J R and Tacey W H 1983 Root occupation and root channels of jarrah forest
subsoils. Australian Journal of Botany 31, 615-627.
Doley D 1967 Water relations of Eucalyptus marginata Sm. under natural conditions.
Journal of Applied Ecology 55, 597-614.
Eberbach P L and Burrows G E 2006 The transpiration response by four topographically
distributed Eucalyptus species, to rainfall occurring during drought in south eastern
Australia. Physiologia Plantarum 127, 483-493.
Enright N J and Lamont B B 1992 Survival, growth and water relations of Banksia
seedlings on a sand mine rehabilitated site and adjacent scrub-heath sites. Journal of
Applied Ecology 29, 663-671.
Fan S, Blake T J and Blumwald E 1994 The relative contribution of elastic and osmotic
adjustments to turgor maintenance of woody species. Physiologia Plantarum 90,
408-413.
Faria T, Silvério D, Breia E, Cabral R, Abadia A, Abadia J, Pereira J S and Chaves M M
1998 Differences in the response of carbon assimilation to summer stress (water
deficits, high light and temperature) in four Mediterranean tree speices. Physiologia
Plantarum 102, 419-428.
79
Farrington P, Turner J V and Gailitis V 1996 Tracing water uptake by jarrah (Eucalyptus
marginata) trees using natural abundances of deuterium. Trees 11, 9-15.
Flexas J, Bota J, Galmés J, Medrano H and Ribas-Carbó M 2006 Keeping a positive carbon
balance under adverse conditions: responses of photosynthesis and respiration to
water stress. Physiologia Plantarum 127, 343-352.
Florence R G 1996 Ecology and silviculture of eucalypt forests. CSIRO Publishing,
Melbourne. pp. 413.
Fordyce I R, Duff G A and Eamus D 1997 The water relations of Allosyncarpia ternata
(Myrtaceae) at contrasting sites in the monsoonal tropics of northern Australia.
Australian Journal of Botany 45, 259-274.
Franks P J, Drake P L and Froend R H 2007 Anisohydric but isohydrodynamic: seasonally
constant plant water potential gradient explained by a stomatal control mechanism
incorporating variable plant hydraulic conductance. Plant, Cell and Environment 30,
19-30.
Grant C D 2006 State-and-transition successional model for bauxite mining rehabilitation
in the jarrah forest of Western Australia. Restoration Ecology 14, 28-37.
Grant C D, Bell D T, Koch J M and Loneragan W A 1996 Implications of seedling
emergence to site restoration following bauxite mining in Western Australia.
Restoration Ecology 4, 146-154.
Grant C D, Norman M A and Smith M A 2007 Fire and silvicultural management of
restored bauxite mines in Western Australia. Restoration Ecology 15, (Supplement)
S127-S136.
Grieve B J 1956 Studies in the water relations of plants. I. Transpiration of Western
Australian sclerophylls. Journal of the Proceedings of the Royal Society of Western
Australia 40, 15-30.
Grigg A M, Veneklaas E J and Lambers H 2008 Water relations and mineral nutrition of
closely related woody plant species on desert dunes and interdunes. Australian
Journal of Botany 56, 27-43.
Gulías J, Flexas J, Abadía A and Medrano H 2002 Photosynthetic responses to water deficit
in six Mediterranean sclerophyll species: possible factors explaining the declining
80
distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species. Tree
Physiology 22, 687-697.
Harris A C 1956 Regeneration of jarrah (Eucalyptus marginata). Australian Forestry 20,
54-62.
Kew G A, Mengler F C and Gilkes R J 2007 Regolith strength, water retention and
implications for ripping and plant root growth in bauxite mine restoration.
Restoration Ecology 15, (Supplement) S54-S64.
Koch J M 2007 Alcoa's mining and restoration process in south Western Australia.
Restoration Ecology 15, (Supplement) S11-S16.
Koch J M and Samsa G P 2007 Restoring Jarrah Forest trees after bauxite mining in
Western Australia. Restoration Ecology 15, (Supplement) S17-S25.
Koch J M, Ward S C, Grant C D and Ainsworth G L 1996 Effects of bauxite mine
restoration operations on topsoil seed reserves in the jarrah forest of Western
Australia. Restoration Ecology 4, 368-376.
Kolb T E and Stone J E 2000 Differences in leaf gas exchange and water relations among
species and tree sizes in an Arizona pine-oak forest. Tree Physiology 20, 1-12.
Körner C and Cochrane P M 1985 Stomatal responses and water relations of Eucalyptus
pauciflora in summer along an elevation gradient. Oecologia 66, 443-455.
Lambers H and Poorter H 1992 Inherent variation in growth rate between higher plants: A
search for physiological causes and ecological consequences. Advances in
Ecological Research 23, 187-261.
Li C 1998 Some aspects of leaf water relations in four provenances of Eucalyptus
microtheca seedlings. Forest Ecology and Management 111, 303-308.
MacFarlane C, White D A and Adams M A 2004 The apparent feed-forward response to
vapour pressure deficit of stomata in droughted, field-grown Eucalyptus globulus
Labill. Plant, Cell and Environment 27, 1268-1280.
Mengler F C, Kew G A, Gilkes R J and Koch J M 2006 Using instrumented bulldozers to
map spatial variation in the strength of regolith for bauxite mine floor rehabilitation.
Soil and Tillage Research 90, 126-144.
81
Merchant A, Callister A, Arndt S, Tausz M and Adams M 2007 Contrasting physiological
responses of six Eucalyptus species to water deficit. Annals of Botany 100, 1507-
1515.
Merchant A, Tausz M, Arndt S K and Adams M A 2006 Cyclitols and carbohydrates in
leaves and roots of 13 Eucalyptus species suggest contrasting physiological
responses to water deficit. Plant, Cell and Environment 29, 2017-2029.
Mott K A and Parkhurst D F 1991 Stomatal response to humidity in air and helox. Plant,
Cell and Environment 14, 509-515.
Ngugi M R, Doley D, Hunt M A, Dart P and Ryan P 2003 Leaf water relations of
Eucalyptus cloeziana and Eucalyptus argophloia in response to water deficit. Tree
Physiology 23, 335-343.
Niinemets Ü 2002 Stomatal conductance alone does not explain the decline in foliar
photosynthetic rates with increasing tree age and size in Picea abies and Pinus
sylvestris. Tree Physiology 22, 515-535.
Passioura J B 2002 Soil conditions and plant growth. Plant, Cell and Environment 25, 311-
318.
Pereira J S, Tenhunen J D and Lange O L 1987 Stomatal control of photosynthesis of
Eucalyptus globulus Labill. trees under field conditions in Portugal. Journal of
Experimental Botany 38, 1678-1688.
Pereira J S, Tenhunen J D, Lange O L, Beyschlag W, Meyer A and David M M 1986
Seasonal and diurnal patterns in leaf gas exchange of Eucalyptus globulus trees
growing in Portugal. Canadian Journal of Forest Research 16, 177-184.
Pook E W, Costin A B and Moore C W E 1966 Water stress in native vegetation during the
drought of 1965. Australian Journal of Botany 14, 257-267.
Prior L D and Eamus D 1999 Seasonal changes in leaf water characteristics of Eucalyptus
tetrodonta and Terminalia ferdinandiana saplings in a northern Australian savanna.
Australian Journal of Botany 47, 587-599.
Prior L D, Eamus D and Duff G A 1997 Seasonal and diurnal patterns of carbon
assimilation. stomatal conductance and leaf water potential in Eucalyptus tetrodonta
saplings in a wet-dry savanna in northern Australia. Australian Journal of Botany
45, 241-258.
82
Ridge R W, Loneragan W A, Bell D T, Colquhoun I J and Kuo J 1984 Comparative studies
in selected species of Eucalyptus used in rehabilitation of the northern jarrah
[Eucalyptus marginata] forest, Western Australia. II. Wood and leaf anatomy.
Australian Journal of Botany 32, 375-386.
Rokich D P, Meney K A, Dixon K W and Sivasithamparam K 2001 The impact of soil
disturbance on root development in woodland communities in Western Australia.
Australian Journal of Botany 49, 169-183.
Rust S and Roloff A 2002 Reduced photosynthesis in old oak (Quercus robur): the impact
of crown and hydraulic architecture. Tree Physiology 22, 597-601.
Sasse J and Sands R 1996 Comparative responses of cuttings and seedlings of Eucalyptus
globulus to water stress. Tree Physiology 16, 287-294.
Stoneman G L, Dell B and Turner N C 1995 Growth of Eucalyptus marginata (jarrah)
seedlings in Mediterranean-climate forest in south-west Australia in response to
overstorey, site and fertiliser application. Forest Ecology and Management 79, 173-
184.
Stoneman G L, Turner N C and Dell B 1994 Leaf growth, photosynthesis and tissue water
relations of greenhouse-grown Eucalyptus marginata seedlings in response to water
deficits. Tree Physiology 14, 633-646.
Szota C, Veneklaas E J, Koch J M and Lambers H 2007 Root architecture of jarrah
(Eucalyptus marginata) trees in relation to post-mining deep ripping in Western
Australia. Restoration Ecology 15, (Supplement) S65-S73.
Thomas D S and Eamus D 1999 The influence of predawn leaf water potential on stomatal
responses to atmospheric water content at constant Ci and on stem hydraulic
coductance and foliar ABA concentrations. Journal of Experimental Botany 50,
243-251.
Tuomela K 1997 Leaf water relations in six provenances of Eucalyptus microtheca: a
greenhouse experiment. Forest Ecology and Management 92, 1-10.
Turner N C 1988 Measurement of plant water status by the pressure chamber technique.
Irrigation Science 9, 289-308.
83
Tyree M T and Hammel H T 1972 The measurement of the turgor pressure and the water
relations of plants by the pressure-bomb technique. Journal of Experimental Botany
23, 267-282.
Varelides C and Kritikos T 1995 Effect of site preparation intensity and fertilisation on
Pinus pinaster survival and height growth on three sites in northern Greece. Forest
Ecology and Management 73, 111-115.
Ward S C, Koch J M and Ainsworth G L 1996 The effect of timing of rehabilitation
procedures on the establishment of a jarrah forest after bauxite mining. Restoration
Ecology 4, 19-24.
Warren C R, Bleby T M and Adams M A 2007 Changes in gas exchange versus leaf solutes
as a means to cope with summer drought in Eucalyptus marginata. Oecologia 154,
1-10.
White D A, Beadle C L and Worledge D 1996 Leaf water relations of Eucalyptus globulus
ssp. globulus and E. nitens: seasonal, drought and species effects. Tree Physiology
16, 469-476.
White D A, Turner N C and Galbraith J H 2000 Leaf water relations and stomatal
behaviour of four allopatric Eucalyptus species planted in Mediterranean
southwestern Australia. Tree Physiology 20, 1157-1165.
Wildy D T, Pate J S and Sefcik L T 2004 Water-use efficiency of a mallee eucalypt
growing naturally and in short-rotation coppice cultivation. Plant and Soil 262, 111-
128.
Zimmermann U and Steudle E 1978 Physical aspects of water relations in plant cells.
Advances in Botanical Research 6, 45-117.
84
Chapter 3. Growth patterns of 13-year-old jarrah (Eucalyptus marginata)
at restored bauxite mine sites in south-western Australia as described by
tree-ring analysis
Abstract
Tree-ring analysis was used to describe development of jarrah (Eucalyptus marginata) trees
over time at low- and high-quality restored bauxite mine sites. Deep-ripping performed
during restoration created crests and troughs (riplines) across the landscape. Tree size on
crests and in riplines was similar at the low-quality site; however, trees on crests at the
high-quality site were 10% shorter and had 26% less basal area than those in riplines.
Trees at the low-quality site showed slow diameter growth rates (1.5-3.4 mm yr-1) from
establishment onwards, presumably as a result of root system restriction in the top 0.5 m of
the soil profile. At the high-quality site, growth rates of trees on crests were slower than
those in riplines over the first three years, presumably due to taproot restriction.
Furthermore, after trees at the high-quality site achieved peak diameter growth rates (7.8
mm yr-1 at age 3 for trees in riplines and 8.1 mm yr-1 at age 5 for trees on crests), trees on
crests had a lower diameter growth rate (1.2-2.7 mm yr-1) than those situated in riplines
(3.6-5.2 mm yr-1). It is likely that trees in riplines will remain the dominant trees in the
stand, while trees on crests will be sub-dominant or suppressed. Ring width was positively
correlated with rainfall received from summer to autumn prior to initiation of diameter
growth for trees on crests (r2=0.51) and in riplines (r2=0.50) at the low-quality site.
Conversely, at the high-quality site, trees on crests (r2=0.73) and in riplines (r2=0.76)
showed a strong positive correlation between ring width and rainfall received from autumn
to spring during the diameter growth phase. Higher responsiveness to rainfall received
early, as opposed to mid-late in the growing season, suggests that the low soil moisture-
storage capacity at the low-quality site was saturated early in the growing season and
therefore additional rainfall did not increase diameter growth.
Introduction
Jarrah (Eucalyptus marginata) is a hardy, evergreen tree species, occurring on the deep
lateritic soils of the Darling Plateau in south-western Australia (Gilkes et al. 1973; Sadlier
85
and Gilkes 1976; Churchward and Dimmock 1989). These lateritic soils are rich in
aluminium hydroxide minerals (Churchward and Dimmock 1989; McArthur 1991), which
are mined as bauxite from the top 2-8 m of the soil profile (Koch 2007). Post-mining
restoration techniques, including deep-ripping, are largely successful at rapidly re-
establishing vegetation across the landscape (Grant et al. 1996; Koch et al. 1996; Ward and
Koch 1996; Koch 2007). ‘Deep-ripping’ or ‘sub-soiling’ (Spoor and Godwin 1978)
involves the pulling or ‘ripping’ of single or multiple tines through the subsoil, with the aim
of relieving compaction in the top 1-2 m of the soil profile. Some materials are not
improved by deep-ripping (Kew et al. 2007), resulting in poor root development (Szota et
al. 2007), and greater water stress (Chapter 2), which results in low-quality forest stands.
Studies of jarrah root morphology (Chapter 1) and seasonal physiology (Chapter 2) give
great insight into what are the current stresses and the trees’ mechanisms for coping with
limitations to growth; however, insights into early stand development require a different
approach. The present study explores whether tree-ring analysis can be used to describe
growth patterns of jarrah saplings (>1.5 m in height and <15 cm diameter at breast height
over bark (Abbott and Loneragan 1984)) over time in response to site quality.
Tree-ring analysis relies on annual events which slow or stop cambial activity to the
point where a distinct ring is evident (Fritts 1976). These annual events are not restricted to
specific climatic zones, as they may include: restriction of water supply (Dunwiddie and
LaMarche 1980; Ash 1983; Stahle et al. 1999; Brienen and Zuidema 2005; Trouet 2006;
Baker et al. 2008), temperature reduction (Dunwiddie and LaMarche 1980; Heinrich and
Banks 2005; Brookhouse and Brack 2006) and intensive insect attack (Readshaw and
Mazanec 1968; Morrow and LaMarche 1978; Wills et al. 2004). Despite initial doubts as
to the application of tree-ring analysis to Eucalyptus species (Ogden 1978), a number of
studies have successfully applied the technique (recently reviewed by Brookhouse (2006)).
The strongly seasonal growth phenology of jarrah, primarily driven by a distinct
summer drought, suits it to tree-ring analysis for the purpose of describing inter-annual
patterns in growth. Jarrah phenology was described by Abbott et al. (1989) as producing
new leaves, which emerge from naked buds in late winter and expand until early summer,
then mature and harden over the summer months. Stem diameter growth occurs from mid-
autumn to early summer (Abbott et al. 1989), prior to any vigorous crown growth (Harris
86
1956). Dense wood with fewer pores (characteristic of the ‘latewood’ found in temperate
northern hemisphere tree species) is produced at the start of the growing season following
break-of-season rainfall in autumn which then gradually changes to light wood with many
pores (‘earlywood’) as growth rates increase during spring (Abbott et al. 1989). This
pattern of wood growth has been referred to as ‘reverse latewood’ (Brookhouse and Brack
2006; 2008), so named as the latewood is formed at the start of, as opposed to the end of
the growing season.
Tree-ring analysis has previously been successfully applied to mature jarrah trees
(~40-400 years old) to develop predictive relationships between diameter at breast height
over bark and tree age in to describe traits of trees, which provide shelter for birds and
mammals (Whitford 2002), fire history (Nicholls 1974; Burrows et al. 1995) and to
correlate annual growth rates with δ13C (Schulze et al. 2006). In the nearby karri
(Eucalyptus diversicolor) forest of south-western Australia, tree-ring analysis has been used
to develop site index predictive growth curves for re-growth karri stands (Rayner 1991).
The present study explores whether tree-ring analysis can be used to describe
growth patterns in young jarrah trees over time at two contrasting restored bauxite mine
sites (low- and high-quality) where soil conditions (Szota et al. 2007) and physiological
functioning (Chapter 2) are distinctly different. The key question underlying this research
was: did trees at the low-quality site always grow slowly, or did growth rates decrease after
an initial period of rapid growth? On the undisturbed forest floor, jarrah seedlings spend
several years accumulating below-ground resources (in lignotubers) prior to initiating major
shoot growth (Abbott and Loneragan 1984). Once the lignotuber is formed, seedlings must
then wait for an opportunity, such as a bushfire or death of a mature tree, to initiate rapid
shoot growth (Harris 1956; Abbott and Loneragan 1984). At high-quality restored bauxite
mines (Ward and Koch 1995; Koch and Ward 2005; Koch and Samsa 2007), recently
logged forest (Abbott and Loneragan 1984) and forest sites where the overstorey has been
removed (Stoneman et al. 1995), initial shoot growth is rapid and the time spent developing
the lignotuber is reduced. It is expected, however, that growth on low-quality sites will not
show rapid initial growth, because the soil constraints will have a larger negative effect on
stand development than the competition from mature trees at high-quality sites.
87
Although mature jarrah retain photosynthetically active leaves during the summer
drought (Colquhoun et al. 1984), presumably because their roots are able to access water
deep in the soil profile (Dell et al. 1983; Farrington et al. 1996), juvenile jarrah cannot
(Bleby 2003; Warren et al. 2007; Chapter 2) and are more likely to reduce growth in years
of low rainfall. A secondary expectation of this study is that annual growth in jarrah will be
related to rainfall, particularly at the low-quality site where, given that access to the subsoil
was restricted (Szota et al. 2007), the water supply of the trees would be drawn from upper
soil layers (Farrington et al. 1996) and therefore be largely dependent on annual rainfall.
Materials and Methods
Study site
This study was carried out between 2003-2005 in a bauxite-mine pit restored in
1992 and located approximately 10 km north-west of Dwellingup (32º43´S, 116º04´E),
Western Australia, Australia. Two 25 m x 50 m plots were established, one in a patch of
small trees, subjectively classed as low-quality, and another in an adjacent area of taller
trees (high-quality) within the same restored pit. Refer to Chapter 1 for a detailed
description of the study site and the restoration process.
Weather data
Weather data presented here were recorded at the township of Dwellingup and supplied by
the Australian Bureau of Meteorology. Dwellingup has a Mediterranean-type climate with
a 72-year average annual rainfall of 1258 mm, with approximately 90% falling between
April and October (Fig. 1). Daily average maximum temperature ranges from ~30°C in
summer to ~15°C in winter, and daily average minimum temperature ranges from ~14°C in
summer to ~5°C in winter (Fig. 1).
Annual rainfall between 1992 and 2004 ranged from 770 to 1407 mm, with an
average of 1189 mm (Fig. 3.1). Annual rainfall fell well below average in three years over
this period, with 943 mm in 1994, 1034 mm in 1997 and 770 mm in 2001. Annual rainfall
was substantially higher than the average in 1992 (1407 mm) and 1996 (1397 mm). Total
rainfall received in the two years (May 2003 – May 2005) between tree growth
measurements was 2303 mm, with 1062 mm received from May – December in 2003, 1163
mm in 2004 and 78 mm received from January – May in 2005.
88
0
500
1000
1500
92 93 94 95 96 97 98 99 00 01 02 03 04Year
Rai
nfal
l (m
m)
Figure 3.1. Annual rainfall from 1992-2004 for Dwellingup (32º43´S, 116º04´E). Data recorded by the Australian Bureau of Meteorology at the Dwellingup weather station (009538), Western Australia, Australia.
Stand characteristics
One large plot (1250 m2) was installed in the centre of the area of interest at each site in
order to quantify both stands. Twenty smaller (100 m2) plots were also installed at each
site in order to develop relationships between stand density and measured tree parameters.
Initial stand characteristics were measured in all plots during May 2003, 11 years after
establishment. Stand density was determined by counting all jarrah and marri trees greater
than 2 m tall in each plot. Tree height was measured for all jarrah trees >2 m tall in each
plot, and recorded as the height of the tallest living section of the crown. Girth over bark at
breast height (1.3 m) was recorded for all stems of all jarrah trees >2 m tall in each plot,
and converted to diameter over bark at breast height (DBH) and basal area over bark at
breast height (BA). In the case of multi-stemmed trees, total tree BA was calculated as the
sum of the BA of all stems >2 m tall. The situation (crest or ripline) of each tree was also
recorded. Thirty pre-selected jarrah trees in each situation at both sites were re-measured in
May 2005 to determine increase in height and BA since 2003. Increases in height and basal
area between 2003 and 2005 were converted to annual growth rates.
Billet preparation
Three jarrah trees representing the median size at each site (low-quality and high-quality)
and situation (crest and ripline) were felled (12 trees sampled in total). Trees were felled at
ground level in May 2005 and the first metre of the bole was air dried for 10 months. A 5-
89
cm thick billet was sawn off each log, such that the assessed transverse surface was 5-15
cm above ground level. Each billet was then sawn in half longitudinally through the centre
in order to observe both the transverse and radial faces. A Japanese-style handsaw with a
thin cut-width (0.3 mm) was used to saw the billets in half to ensure that the growth rings
closest to the centre were not lost as a result of the cut.
Transverse and radial faces of each section were initially sanded with 120 grit
sandpaper using an orbital sander to remove saw marks. Billets were then sanded by hand
with increasingly finer sandpaper, ranging from 120, 360, 800, 1200 grit to finish with
2000 grit sandpaper, which essentially polished the billet. Growth rings became clearer,
particularly on the radial face of each section, once the finest grade of sandpaper was used
for considerable time (average sanding time ~2 hrs per face) to remove marks made by the
previous grade of sandpaper.
Tree-rings of all samples showed a ‘reverse latewood’ pattern, similar to that
observed in Eucalyptus obliqua Ľ.Hérit, E. sieberi L.A.S. Johnson, E. cypellocarpa L.A.S.
Johnson, and E. baxteri (Benth.) Maiden & Blakely ex J.M. Black (Brookhouse and Brack
2006; 2008), where dark latewood laid down at the start of the growing season in autumn
gradually changed to lighter ‘earlywood’ as growth rates increased during spring. In some
samples, a band of latewood was evident at the end of the season’s growth which produced
a ‘false ring’, making assessments on the transverse face difficult. This problem was
overcome by measuring ring width on the radial face of each billet, where changes in wood
colour were not as dramatic within a season and false rings could be eliminated as they
were faint, absent or unrecognisable at both ends of the radial face (Alcorn et al. 2001). It
was therefore possible to confidently identify annual growth rings, which were marked by a
distinctive narrow line. Ring widths were quantified through visual assessment of the
radial face of each billet using a dissection microscope at 20X-40X magnification. Water
was applied to each surface to increase contrast between growth rings and the surrounding
wood. Pins were used to mark the location of growth rings and a vernier caliper was used
to measure ring widths. Two radii were measured on each radial face of each halved billet
such that a total of 4 radii were measured per billet. Twelve growth rings were evident on
each sample, the inner-most of which was assumed to have been laid down during the first
winter (1992). A small band of dark wood was evident between the 12th ring and the
90
exterior of the sapwood which was assumed to be the cambial growth laid down between
break-of-season rainfall in March 2005 and the time of felling in May 2005. As this last
ring was incomplete it was not included in the analyses that follow.
Cross-dating is an integral part of dendrochronological studies and refers to the
process of correlating tree ring patterns between specimens (Fritts 1976). This technique is
essential when comparing trees of unknown age; however, it was also a useful technique in
the present study where tree age was known. Samples were cross-dated to ensure that trees
at the low-quality site were indeed the same age as those at the high-quality site; and that
they had not germinated several years after trees at the high-quality site. Given the
broadcast seeding method of jarrah forest restoration, it is possible that not all seeds
germinated in the first year. Correct dating was confirmed by the 1997 and 2001 growth
rings, which were consistently the smallest rings, presumably a result of dry growing
conditions.
Data analyses
Two-way analysis of variance (ANOVA) was used to test for significant differences
between site (low-quality and high-quality) and situation (crest and ripline) for the stand
characteristics (height, basal area, height growth rates and basal area growth rates). Two-
way ANOVA was also used to test for significant differences in annual tree ring width
between site and situation within a given year. One-way ANOVA was used to test for
significant differences between years within site and situation. Linear regression analysis
was used to determine the relationships between stand density and tree basal area, tree
height and tree diameter at breast height over bark. Linear regression analysis was also
used to determine the relationship between tree-ring width and rainfall, minimum
temperature, maximum temperature and vapour pressure deficit for different seasons and
groups of seasons. All data were tested for normality using a Shapiro-Wilk test and log-
transformations were performed where appropriate).
91
Results
Stand characteristics
The low-quality site had 1680 stems ha-1 (80% jarrah and 20% marri) compared with 4264
stems ha-1 at the high-quality site (76% jarrah and 24% marri) (Table 3.1). The majority of
jarrah and marri trees at both sites were located in riplines (60% at the low-quality site and
63% at the high-quality site) as opposed to on crests.
Jarrah trees on crests at the low-quality site were 39% shorter and had 13% less
basal area compared with those at the high-quality site (Table 3.1). Jarrah trees in riplines
at the low quality site were 46% shorter with 48% less basal area than those at the high-
quality site. There was no significant difference in either height or basal area between
jarrah growing on crests or in riplines at the low-quality site. Jarrah trees growing on crests
at the high-quality site were 10% shorter and had 26% less basal area than those growing in
riplines.
Tree height growth rates (2003-2005) were similar for jarrah on crests and in
riplines at the low-quality site (Table 3.1). Annual height growth rates of jarrah on crests at
the high-quality site were 48% greater than those at the low-quality site. Jarrah in riplines
showed 59% higher height growth rates than those on crests at the high-quality site. Jarrah
in riplines at the high-quality site had 41%, 62% and 47% higher annual basal area growth
rates than those on crests and in riplines at the low-quality site, and those on crests at the
high-quality site.
Annual tree-ring patterns (1992-2004)
Annual growth rates of trees at the low-quality site remained fairly constant since
establishment, while growth rates at the high-quality site were higher in the first 5 years and
declined thereafter (Fig. 3.2). There were no differences in the pattern or magnitude of
growth rings of trees on crests or in riplines at the low-quality site. There were two major
differences in the growth of trees on crests compared with trees in riplines at the high-
quality site. Firstly, trees on crests had slower growth in the first three years compared with
trees in riplines. Secondly, following peak growth rates (achieved at age 5 for trees on
crests and age 3 for trees in riplines), growth rates declined significantly for trees on crests
and remained high for trees in riplines.
92
Table 3.1. Stand and tree characteristics of jarrah (Eucalyptus marginata) at low- and high-quality restored bauxite mine sites (mean standard error in parentheses with n = number of jarrah trees). Mean annual growth rates (2003-2005) for height and basal area per tree (n=30 trees per treatment) are also presented, with mean standard error in parentheses. Within rows, different letters indicate significant differences (P < 0.05) between site and situation. P-value refers to the interaction site*situation (two-way ANOVA).
Site Low-quality Low-quality High-quality High-quality
Tree situation Crest Ripline Crest Ripline P-value
Number of trees 70 98 160 247
Height (m) 4.6 (± 0.2)a 4.5 (± 0.1)a 7.5 (± 0.2)b 8.3 (± 0.1)c 0.01
Basal area (cm2) 95.0 (± 9.0)a 77.7 (± 5.6)a 109.6 (± 6.5)b 148.4 (± 6.4)c <0.001
Height growth rate
(m year-1)
0.40 (± 0.05)a 0.45 (± 0.04)a 0.59 (± 0.03)b 0.94 (± 0.05)c 0.01
Basal area growth
rate (cm2 year-1)
21.9 (± 1.9)a 19.1 (± 1.3)a 21.0 (± 1.5)a 30.9 (± 2.1)b <0.001
0
2
4
6
8
10
12
92 93 94 95 96 97 98 99 00 01 02 03 04Year
Rin
g w
idth
(mm
)
Figure 3.2. Annual tree-ring width for jarrah (Eucalyptus marginata) situated on crests (squares) and in riplines (circles) at low-quality (solid) and high-quality (open) restored bauxite mine sites. Bars on means represent mean standard error (n=3). Bold bars indicate significant differences within years for the interaction site*situation (two-way ANOVA).
93
Relationships between tree size and stand density
There was no significant relationship between tree size (basal area or tree height) and stand
density for trees on crests at the low-quality site (Figs. 3.3A and 3.3C). There was a weak
negative relationship between tree basal area and stand density for trees in riplines at the
low-quality site (Fig. 3.3A), yet no relationship between tree height and stand density (Fig.
3.3C). In contrast, for trees on crests at the high-quality site there was a strong negative
relationship between tree basal area and stand density, while trees in riplines showed a
weak negative relationship (Fig 3.3B). Neither trees on crests nor trees in riplines at the
high-quality site showed any relationship between tree height and stand density (Fig. 3.3B).
Figure 3.3. Relationship between stand density and tree basal area (A and B) and tree height (C and D) for jarrah (Eucalyptus marginata) trees situated on crests (squares) and in riplines (circles) at low-quality (solid) and high-quality (open) restored bauxite mine sites. Measurements were taken 11 years post-establishment in May, 2003 from twenty 100 m2
plots at each site. Each point represents the average value of each parameter from each measurement plot. Bars on values represent mean standard error (n=20). Tree-ring width and climate
0
50
100
150
200
250
300
0 1500 3000 4500 6000 7500Stand density (trees ha-1)
Bas
al a
rea
(cm
2 tree
-1)
Crest y = -0.021x + 200 r2 = 0.76
Rip y = -0.019x + 226, r2 = 0.54
0
50
100
150
200
250
300
0 1500 3000 4500 6000 7500Stand density (trees ha-1)
Bas
al a
rea
(cm
2 tree
-1)
Crest y = -0.046x + 165, r2 = 0.45
Rip y = -0.046x + 168, r2 = 0.65
0
5
10
15
0 1500 3000 4500 6000 7500
Stand density (trees ha-1)
Hei
ght (
m)
Rip y = -0.0002x + 9.2, r2 = 0.18
Crest y = -0.0001x + 8.1, r2 = 0.040
5
10
15
0 1500 3000 4500 6000 7500
Stand density (trees ha-1)
Hei
ght (
m)
Crest y = -0.0008x + 5.9, r2 = 0.20
Rip y = -0.0013x + 7.1, r2 = 0.40
A
C
B
D
0
50
100
150
200
250
300
0 1500 3000 4500 6000 7500Stand density (trees ha-1)
Bas
al a
rea
(cm
2 tree
-1)
Crest y = -0.021x + 200 r2 = 0.76
Rip y = -0.019x + 226, r2 = 0.54
0
50
100
150
200
250
300
0 1500 3000 4500 6000 7500Stand density (trees ha-1)
Bas
al a
rea
(cm
2 tree
-1)
Crest y = -0.046x + 165, r2 = 0.45
Rip y = -0.046x + 168, r2 = 0.65
0
5
10
15
0 1500 3000 4500 6000 7500
Stand density (trees ha-1)
Hei
ght (
m)
Rip y = -0.0002x + 9.2, r2 = 0.18
Crest y = -0.0001x + 8.1, r2 = 0.040
5
10
15
0 1500 3000 4500 6000 7500
Stand density (trees ha-1)
Hei
ght (
m)
Crest y = -0.0008x + 5.9, r2 = 0.20
Rip y = -0.0013x + 7.1, r2 = 0.40
A
C
B
D
94
Tree-ring width was correlated with total rainfall, average maximum and minimum
temperature and average vapour pressure deficit (VPD; an estimation of evaporative
demand from the atmosphere) of seasons (and groups of seasons) from the previous and the
current year (year of tree-ring production).
Trees on crests and in riplines at the low-quality site showed a weak positive
relationship between ring width and rainfall received between the start of the previous
summer and the end of the current autumn (Fig. 3.4A); while trees at the high-quality site
showed no relationship (Fig. 3.4B). There was, however, a strong positive relationship
between ring width and rainfall received from autumn to spring in the current year for trees
on crests and in riplines at the high-quality site (Fig. 3.4D), but not at the low-quality site
(Fig. 3.4C). There was no significant relationship between ring width and annual rainfall
for trees on crests or in riplines at the low-quality site. Positive relationships between ring
width and annual rainfall remained for trees on crests and in riplines at the high-quality site;
however, the strength of the relationship was lower for trees on crests (r2=0.67) and in
riplines (r2=0.74) than for the correlation for rainfall received from autumn to spring. Ring
width was 41% and 37% smaller in the driest year (2001; 770 mm) compared with the
wettest year (1999; 1323 mm) for trees on crests and in riplines at the high-quality site.
Years with low average minimum temperatures during autumn and winter produced
the smallest annual growth rings for trees on crests and in riplines at both sites (Figs. 3.5A
and 3.5B). Trees on crests at both sites showed no correlation between ring width and
average maximum temperature; however, trees in riplines at both sites showed weak
negative relationships between ring width and average maximum temperature of the
previous spring (Figs. 3.5C and 3.5D). There was no significant correlation between ring
width and vapour pressure deficit (VPD) for trees at either site for any individual month,
season or groups of seasons analysed.
95
Figure 3.4. Relationship between annual tree-ring width and rainfall received between the previous summer and current autumn (A and B); and relationship between tree-ring width and rainfall received between autumn and spring in the current year (C and D) for jarrah (Eucalyptus marginata) situated on crests (squares) and in riplines (circles) at low-quality (solid) and high-quality (open) restored bauxite mine sites. Only data from 1997-2004 (tree age ≥5 years old) are shown. Bars represent mean standard error (n=3).
01234567
0 500 1000 1500
Rainfall (mm)
Rin
g w
idth
(mm
)
Rip y = 0.001x + 0.39, r 2 = 0.39
Crest y = 0.002x + 0.17, r 2 = 0.47
01234567
0 100 200 300 400
Rainfall (mm)
Rin
g w
idth
(mm
)
Rip y = 0.003x + 1.16, r 2 = 0.50
Crest y = 0.005x + 0.87, r 2 = 0.51
01234567
0 500 1000 1500
Rainfall (mm)
Rin
g w
idth
(mm
)Crest y = 0.002x - 0.35, r 2 = 0.73
Rip y = 0.003x + 0.49, r 2 = 0.76
01234567
0 100 200 300 400
Rainfall (mm)
Rin
g w
idth
(mm
) Rip y = 0.006x + 2.69, r 2 = 0.33
Crest y = 0.003x + 1.29, r 2 = 0.20
B
A C
D
01234567
0 500 1000 1500
Rainfall (mm)
Rin
g w
idth
(mm
)
Rip y = 0.001x + 0.39, r 2 = 0.39
Crest y = 0.002x + 0.17, r 2 = 0.47
01234567
0 100 200 300 400
Rainfall (mm)
Rin
g w
idth
(mm
)
Rip y = 0.003x + 1.16, r 2 = 0.50
Crest y = 0.005x + 0.87, r 2 = 0.51
01234567
0 500 1000 1500
Rainfall (mm)
Rin
g w
idth
(mm
)Crest y = 0.002x - 0.35, r 2 = 0.73
Rip y = 0.003x + 0.49, r 2 = 0.76
01234567
0 100 200 300 400
Rainfall (mm)
Rin
g w
idth
(mm
) Rip y = 0.006x + 2.69, r 2 = 0.33
Crest y = 0.003x + 1.29, r 2 = 0.20
B
A C
D
96
Figure 3.5. Relationship between annual tree-ring width and average monthly minimum temperature during the current autumn and winter (A and B); and relationship between annual tree-ring width and average maximum temperature of the previous spring (C and D) for jarrah (Eucalyptus marginata) situated on crests (squares) and in riplines (circles) at low-quality (solid) and high-quality (open) restored bauxite mine sites. Only data from 1997-2004 (tree age ≥5 years old) are shown. Bars represent mean standard error (n=3).
Discussion
Tree-ring patterns and stand development
Tree-ring analysis revealed that trees at the low-quality site showed slower annual growth
rates compared with those at the high-quality site. This was most likely due to restriction
of root systems to the top 0.5 m (Szota et al. 2007) resulting in severe summer water stress
(Chapter 2) at the low-quality site. Results presented in Chapter 2 showed that severe water
stress decreased photosynthetic rates during drought, resulting in cessation of growth earlier
in the growing season. Basal area growth rates at the low-quality site (21.9 and 19.1 cm2
yr-1 for trees on crests and in riplines) were significantly slower than for trees in riplines at
the high-quality site (30.9 cm2 yr-1), but were similar to those found by Bleby (2003) at
younger (~age 7) nearby restored bauxite mine sites (~20 cm yr-1). Abbott and Loneragan
(1983a) showed that diameter increments of low-quality mature, cut-over jarrah forest
01234567
19 20 21 22 23
Rainfall (mm)
Rin
g w
idth
(mm
)
Rip y = -0.44x + 11.3, r 2 = 0.65
Crest y = -0.23x + 7.0, r 2 = 0.06
01234567
7 8 9 10
Rainfall (mm)
Rin
g w
idth
(mm
)Rip y = 0.35x - 1.00, r 2 = 0.52
Crest y = 0.59x - 2.76, r 2 = 0.54
01234567
19 20 21 22 23
Max. Temperature (°C)
Rin
g w
idth
(mm
)Crest y = -0.38x + 10.0, r 2 = 0.19
Rip y = -0.96x + 24.4, r 2 = 0.55
01234567
7 8 9 10
Min. Temperature (°C)
Rin
g w
idth
(mm
) Rip y = 0.97x - 4.03, r 2 = 0.72
Crest y = 0.56x - 2.63, r 2 = 0.53
B
A C
D
01234567
19 20 21 22 23
Rainfall (mm)
Rin
g w
idth
(mm
)
Rip y = -0.44x + 11.3, r 2 = 0.65
Crest y = -0.23x + 7.0, r 2 = 0.06
01234567
7 8 9 10
Rainfall (mm)
Rin
g w
idth
(mm
)Rip y = 0.35x - 1.00, r 2 = 0.52
Crest y = 0.59x - 2.76, r 2 = 0.54
01234567
19 20 21 22 23
Max. Temperature (°C)
Rin
g w
idth
(mm
)Crest y = -0.38x + 10.0, r 2 = 0.19
Rip y = -0.96x + 24.4, r 2 = 0.55
01234567
7 8 9 10
Min. Temperature (°C)
Rin
g w
idth
(mm
) Rip y = 0.97x - 4.03, r 2 = 0.72
Crest y = 0.56x - 2.63, r 2 = 0.53
B
A C
D
97
stands were 57% of those at high-quality stands which is approximately the magnitude by
which trees in riplines at the high-quality site were out-growing trees at the low-quality site
in the last years prior to sampling.
Trees at the low-quality site demonstrated slow growth rates from the first year
onwards, unlike trees at the high-quality site which showed faster growth rates in the first 5
years which subsequently declined with age. This result suggests that tree growth at the
low-quality site was restricted from as early as the first year post-establishment. Severe
limitations to root growth at this site (Chapter 1), combined with the presumed lower soil-
moisture capacity, may have subjected the trees to high water stress, causing initial
mortality, which may explain the observed lower stocking rate. Results from the present
study indicate that a subsoil constraint in the top 0.5 m (Chapter 1) will restrict the primary
root growth of jarrah trees as early as the first year of growth. Several eucalypts have
demonstrated the ability to develop vertical roots rapidly in their first year: Eucalyptus
globulus Labill. seedlings in southern Tasmania reached depths exceeding 0.5 m after 3-6
months (O'Grady et al. 2005); hybrid eucalypt clones (Eucalyptus PF1 clone 1-41) in the
Pointe-Noire region of Congo reached 3 m depth in the first year (Bouillet et al. 2002); and
the roots of Eucalyptus grandis Hill ex Maiden in a mixed stand in Kenya reached 3.95 m
after only 11 months (Jama et al. 1998). Above-ground growth of jarrah seedlings in the
undisturbed forest is only triggered once below-ground resources (lignotuber and root
system) develop to a sufficient size (Abbott and Loneragan 1984), with seedlings often
reaching a height of only 6-8 cm after 10 years. Once below-ground resources reach a
critical size (the exact size is unknown but generally thought to be when the lignotuber is
~10 cm in diameter (Harris 1956)), relatively rapid shoot growth is stimulated. At restored
sites, in the absence of competition from mature trees (Stoneman et al. 1995), and where
resources including light, temperature and moisture are not limiting (Stoneman and Dell
1993; Stoneman et al. 1994; Stoneman et al. 1995); seedlings bypass this below-ground
development phase and demonstrate rapid above-ground growth (Abbott and Loneragan
1984). Jarrah at restored sites can grow >3 m tall in the first 4-5 years (Ward and Koch
1995) and achieve 9 m in 13 years (Koch and Ward 2005); with 1 m yr-1 considered to be
the average for young restored sites (Koch and Samsa 2007). Despite the fact that jarrah
seedlings on restored sites do not develop a lignotuber before initiating shoot growth,
98
results from the present research suggest that an inherent link between above- and below-
ground development is maintained, reflected by the fact that where below-ground
development is restricted, above-ground growth rates are substantially reduced. Shea et al.
(1975) and later Dell et al. (1983) did not find this response for eastern Australian eucalypts
(E. microcorys, E. resinifera, E. maculata, E. saligna and E. globulus) planted at restored
bauxite mines; instead finding that above-ground growth was disproportionately higher that
below-ground growth; a pattern of development not conducive to long-term survival
(Lambers and Poorter 1992). The ability of jarrah to keep shoot growth ‘in check’ with
root growth may partially explain its success at colonising a large, heterogeneous
geographical range (Brooker and Kleinig 2001) and may enhance its survival at low-quality
restored mine sites.
Growth of trees on crests was slower for the first three years compared with those in
riplines at the high-quality site, a difference that is probably also related to differences in
root system development. Trees on crests at the high-quality site had higher proportions of
root cross-sectional area in lateral and sinker roots than in the taproot, a pattern that was
similar to trees at the low-quality site (Szota et al. 2007). The delay in achieving peak rates
of growth for trees in crests indicates that it took 3 years for these trees to gain adequate
access to the subsoil and therefore increase growth rates to levels comparable with trees
situated on riplines. Growth of trees in riplines was unimpeded in the first 3 years, most
likely as a result of the deep-ripping process improving soil structure (Spoor and Godwin
1978; Croton and Watson 1987; Kew et al. 2007).
Diameter growth of jarrah saplings at restored sites averages ~1 cm yr-1 (Koch and
Samsa 2007), compared to 0.1-0.2 cm yr-1 for mature jarrah (Harris 1956; Abbott and
Loneragan 1983a). Diameter growth at the high-quality site, as estimated from tree-ring
width, slowed considerably since the peak of growth and varied between ~0.4-0.5 cm yr-1.
This relatively slow diameter growth rate may indicate that inter-tree competition as a
result of the unusually high stocking (4264 stems ha-1; approximately double the average
stocking density at restored sites (Koch and Ward 2005)) at the high-quality site is causing
growth rates to decline and will prevent maturation of the stand (Assmann 1970; Florence
1996). Koch and Ward (2005) found a negative relationship between diameter increment
and stand density at restored stands with ~1000-4000 stems ha-1. Jarrah forest stands,
99
including those at restored mine sites, have unusually low mortality rates, even when
heavily over-stocked. For example, Koch and Ward (2005) recorded 84% survival at a
stand stocked at 4875 stems ha-1 at age 13 years. Inter-tree competition for resources
causes all trees to be smaller, rather than increasing mortality (Stoneman et al. 1989; Koch
and Ward 2005). In the present study, slow annual diameter growth rates, combined with a
negative relationship between tree basal area and stand density, indicate that the high-
quality site may require thinning in order to increase tree size and promote stand
development (Stoneman and Whitford 1995; Koch and Samsa 2007). Grant et al. (2007)
showed a positive response to thinning at a 10-13 year old restored stand (originally
stocked at 1756 stems ha-1), which was thinned to 400-625 stems ha-1, causing a 4-fold
increase in the diameter increment of retained stems after 18 months.
Thinning methods can maximise wood production (Florence 1996) or provide non-
wood production benefits such as promoting biodiversity (Cummings and Reid 2008). To
promote timber production, trees on crests should be removed since they are the
intermediate, overtopped and suppressed trees in the stand; and their removal will boost the
growth of dominant trees in riplines (Florence 1996). Furthermore, trees in riplines have
more direct access to subsoil than those on crests (Szota et al. 2007), and have a greater
likelihood of surviving periods of extended drought. Trees in riplines are also at an
advantage nutritionally, as leaf litter and therefore nutrients tend to concentrate in the
ripline (Todd et al. 2000; Ward 2000). On the other hand, non-selective tree thinning is
more likely to increase the diversity of the canopy and broaden the size class distribution of
the stand (Florence 1996), making it more closely resemble an unmined forest stand
(Abbott and Loneragan 1983b; Abbott 1984). Root system studies by Szota et al. (2007)
showed that trees on crests had fewer lateral roots (1-3) compared with trees in riplines (4-
6) which suggests that trees on crests have a greater susceptibility to windthrow (Coutts
1983; Mickovski and Ennos 2002), increasing the number of habitat logs for wildlife on the
forest floor. Non-selectively thinning to a stand density of 1000 - 1500 stems ha-1 should
restore both the required timber and biodiversity resource of the forest. Target stand
density at restored bauxite mines has been reduced to 1300 stems ha-1 (at age 9 months) in
recent years (Grant 2006) which is more likely to restore the timber production and
ecological functioning value of the original forest.
100
Tree-ring patterns and climate
The influence of site and situation on growth rates was obviously stronger than that of
climatic variables during the first five years after establishment; therefore correlations
between tree-ring widths and rainfall, temperature and VPD were made from 1997 (age 5)
onwards.
Tree-ring width was greater in years in which higher rainfall was received during
the summer and autumn immediately prior to commencement of diameter growth for trees
at the low-quality site, rather than in years where high rainfall was received during the main
phase of diameter growth (mid-autumn to early summer) for jarrah (Abbott et al. 1989).
One explanation for this finding is that shallow soil depth and presumed low soil moisture-
storage capacity at the low-quality site reached maximum moisture-storage early in the
growing season, even in years with low rainfall, and therefore higher rainfall received
during the growing season did not increase water availability and diameter growth. This
was unexpected, as species on shallow soils typically have a higher dependence on rainfall
than those with greater soil depth (Eberbach and Burrows 2006). The strong positive
relationship between ring width and rainfall received during the diameter growth phase in
trees at the high-quality site suggests that, despite greater root depth and presumed higher
soil-moisture-storage capacity, pressure on water resources as a result of the high stand
density (4264 stems ha-1) resulted in diameter growth being strongly dependent on rainfall
received during the growth phase. Although ring width at the two sites depended on
rainfall received at different times of the year at the two sites, it is clear that recent rainfall
is a key driver of annual diameter growth.
Rainfall is a key determinant of annual diameter growth for both deciduous and
evergreen species, even at high-rainfall sites with low intra-annual variation. Eucalyptus
globulus in Portugal showed a positive correlation between tree-ring width and annual
rainfall on low rainfall sites (535 mm yr-1) but not on high rainfall sites (1108 mm yr-1)
(Leal et al. 2004). Heinrich and Banks (2005) found a positive correlation between ring
width and rainfall received at the end of the growing season (March to May) for the
deciduous Australian red cedar (Toona ciliata) at a high-rainfall (1439 mm yr-1) site with
evenly distributed rainfall over the year. Ash (1983) and Baker et al. (2008) demonstrated
positive correlations between diameter growth and rainfall received during the wet season
101
for Callitris spp. in the northern tropics of Australia. Ring width also increased in wet
years in Pinus spp. growing in northern Arizona (Adams and Kolb 2004). Ring width in
beech (Fagus sylvatica) growing in the seasonally dry Abruzzo region of Italy (1180 mm
yr-1) was positively correlated with rainfall received in early summer which prolonged the
diameter growth increment, but not with rainfall received prior to (late winter) or during
(spring) rapid initial diameter growth (Skomarkova et al. 2006). In contrast, ring width in
beech in Germany (750-800 mm yr-1) with little annual variation in rainfall was positively
correlated with rainfall received in late winter and spring prior to initiation of diameter
growth (Skomarkova et al. 2006).
Several authors have found correlations between annual diameter growth and
rainfall, maximum temperature or VPD from the year preceding year as opposed to the
current year, which may be related to the quantity of photosynthates accumulated in the
spring/summer prior to initiation of diameter growth. Macfarlane and Adams (1998) found
a strong positive correlation between diameter growth and annual rainfall from the previous
year in E. globulus from a low-rainfall site (640 mm yr-1) in south-western Australia. High
temperature or VPD in spring or summer as soil moisture declines can induce stomatal
closure early in the dry season (Chapter 3) which can potentially limit the amount of
photosynthates captured, and therefore the resources available for diameter growth in
autumn. The negative relationships between ring width and maximum temperature of the
previous spring in the present study were found for trees in riplines at both sites, but not for
trees on crests; therefore it is not possible to conclude that high maximum temperatures
reduced the amount of photosynthates captured. Carbon- and/or oxygen-isotope analysis
(Macfarlane and Adams 1998; Pate and Arthur 1998; Schulze et al. 2006; Cullen and
Grierson 2007) of wood within and between years would provide further insight into the
impact of temperature and/or VPD on the seasonal wood production of young jarrah trees.
Low minimum temperatures in the autumn and spring had a similar impact on
diameter growth of trees at both sites, where smaller diameter growth occurred in years
with low autumn and winter minimum temperatures, which is a common feature of
eucalypts from high altitudes or cold climates (Brookhouse and Brack 2006), but also
occurs in species from the tropical north of Australia (Baker et al. 2008).
102
Conclusions
The present study has shown that initial growth of jarrah is strongly dependent on soil
conditions and that a constraint in the top 0.5 m of the soil profile will limit productivity
from as early as the first year of growth. Growth of trees at sites with low soil moisture-
storage capacity was more responsive to rainfall early in the year; while growth of trees at
sites with a high capacity to store soil moisture was more dependent on rainfall received
during and towards the end of the diameter growth phase. High maximum temperature in
spring prior to diameter growth decreased tree-ring width, as did low minimum
temperatures during autumn and winter.
Previous studies that identified annual patterns in eucalypts exhibiting ‘reverse-
latewood’ (Brookhouse and Brack 2006; 2008) greatly improved confidence in applying
the technique to young jarrah trees. Tree-ring analysis of jarrah shows great potential as a
tool to describe the development of young trees, particularly those exposed to severe
summer drought, and would benefit significantly from further anatomical and physiological
studies such as those carried out for Eucalyptus globulus (Macfarlane and Adams 1998;
Pate and Arthur 1998; Leal et al. 2004) and other eucalypts (Akeroyd et al. 2002; Schulze
et al. 2006).
References
Abbott I 1984 Comparisons of spatial pattern, structure, and tree composition between
virgin and cut-over jarrah forest in Western Australia. Forest Ecology and
Management 9, 101-126.
Abbott I, Dell B and Loneragan O 1989 The jarrah plant. In The jarrah forest: a complex
Mediterranean ecosystem. Eds. B Dell, J J Havel and N Malajczuk. pp 41-51.
Kluwer Academic Publishers, Dordrecht.
Abbott I and Loneragan O 1983a Growth rate of jarrah (Eucalyptus marginata) in relation
to site quality in cut-over forest, Western Australia. Australian Forestry 46, 91-102.
Abbott I and Loneragan O 1983b Response of jarrah (Eucalyptus marginata) regrowth to
thinning. Australian Forest Research 13, 217-229.
103
Abbott I and Loneragan O 1984 Growth rate and long-term population dynamics of jarrah
(Eucalyptus marginata Donn ex Sm.) regeneration in Western Australian forest.
Australian Journal of Botany 32, 353-362.
Adams H D and Kolb T E 2004 Drought responses of conifers in ecotone forests of
northern Arizona: tree ring growth and leaf δ13C. Oecologia 140, 217-225.
Akeroyd M D, Leaney F W, Mathieson M, Moloney D and Smith G C 2002 Dating spotted
gum (Corymbia citriodora) tree rings in south-eastern Queensland using 14C
measurements of cellulose. Australian Forestry 65, 265-267.
Alcorn P J, Dingle J K and Hickey J E 2001 Age and stand structure in a multi-aged wet
eucalypt forest at the Warra silvicultural systems trial. Tasforests 13, 245-259.
Ash J 1983 Tree rings in tropical Callitris macleayana F. Muell. Australian Journal of
Botany 31, 277-281.
Assmann E 1970 The principles of forest yield study. Pergamon Press, Oxford. pp. 506.
Baker P J, Palmer J G and D'Arrigo R 2008 The dendrochronology of Callitris intratropica
in northern Australia: annual ring structure, chronology development and climate
correlations. Australian Journal of Botany 56, 311-320.
Bleby T M 2003 Water use, ecophysiology and hydraulic architecture of Eucalyptus
marginata (jarrah) growing on mine rehabilitation sites in the jarrah forest of south-
western Australia. PhD Thesis, The University of Western Australia, Perth.
Bouillet J-P, Laclau J-P, Arnaud M, M'Bou A T, Saint-André L and Jourdan C 2002
Changes with age in the spatial distribution of roots of Eucalyptus clone in Congo -
Impact on water and nutrient uptake. Forest Ecology and Management 171, 43-57.
Brienen R J W and Zuidema P A 2005 Relating tree growth to rainfall in Bolivian rain
forests:a test for six species using tree ring analysis. Oecologia 146, 1-12.
Brooker M I H and Kleinig D A 2001 Field guide to eucalypts. Vol. 2, South-western and
southern Australia. Bloomings Books, Melbourne. pp. 428.
Brookhouse M 2006 Eucalypt dendrochronology: past, present and potential. Australian
Journal of Botany 54, 435-449.
Brookhouse M and Brack C 2006 Crossdating and analysis of eucalypt tree rings exhibiting
terminal and reverse latewood. Trees 20, 767-781.
104
Brookhouse M and Brack C 2008 The effect of age and sample position on eucalypt tree-
ring width series. Canadian Journal of Forest Research 38, 1144-1158.
Burrows N D, Ward B and Robinson A D 1995 Jarrah forest fire history from stem analysis
and anthropological evidence. Australian Forestry 58, 7-16.
Carbon B A, Bartle G A and Murray A M 1981 Patterns of water stress and transpiration in
jarrah (Eucalyptus marginata Don ex Sm.) forests. Australian Forest Research 11,
191-200.
Churchward H M and Dimmock G M 1989 The soils and landforms of the northern jarrah
forest. In The jarrah forest: a complex Mediterranean ecosystem. Eds. B Dell, J J
Havel and N Malajczuk. pp 13-21. Kluwer Academic Publishers, Dordrecht.
Colquhoun I J, Ridge R W, Bell D T, Loneragan W A and Kuo J 1984 Comparative studies
in selected species of Eucalyptus used in rehabilitation of the northern jarrah forest,
Western Australia. I. Patterns of xylem pressure potential and diffusive resistance of
leaves. Australian Journal of Botany 32, 367-373.
Coutts M P 1983 Root architecture and tree stability. Plant and Soil 71, 171-188.
Croton J T and Watson G D 1987 Mining related compaction - a case study in the Darling
Range, Western Australia. pp 1-19. ALCOA World Alumina Australia, Perth, W.A.
Cullen L E and Grierson P F 2007 A stable oxygen, but not carbon, isotope chronology of
Callitris columellaris reflects recent climate change in north-western Australia.
Climatic Change 85, 213-229.
Cummings J and Reid N 2008 Stand-level management of plantations to improve
biodiversity values. Biodiversity Conservation 17, 1187-1211.
Dell B, Bartle J R and Tacey W H 1983 Root occupation and root channels of jarrah forest
subsoils. Australian Journal of Botany 31, 615-627.
Dunwiddie P W and LaMarche V C, Jr. 1980 Dendrochronological characteristics of some
native Australian trees. Australian Forestry 43, 124-135.
Eberbach P L and Burrows G E 2006 The transpiration response by four topographically
distributed Eucalyptus species, to rainfall occurring during drought in south eastern
Australia. Physiologia Plantarum 127, 483-493.
Farrington P, Turner J V and Gailitis V 1996 Tracing water uptake by jarrah (Eucalyptus
marginata) trees using natural abundances of deuterium. Trees 11, 9-15.
105
Florence R G 1996 Ecology and silviculture of eucalypt forests. CSIRO Publishing,
Melbourne. pp. 413.
Fritts H C 1976 Tree rings and climate. Academic Press, London. pp. 567.
Gilkes R J, Scholz G and Dimmock G M 1973 Lateritic deep weathering of granite. Journal
of Soil Science 24, 523-536.
Grant C D 2006 State-and-transition successional model for bauxite mining rehabilitation
in the jarrah forest of Western Australia. Restoration Ecology 14, 28-37.
Grant C D, Bell D T, Koch J M and Loneragan W A 1996 Implications of seedling
emergence to site restoration following bauxite mining in Western Australia.
Restoration Ecology 4, 146-154.
Grant C D, Norman M A and Smith M A 2007 Fire and silvicultural management of
restored bauxite mines in Western Australia. Restoration Ecology 15, (Supplement)
S127-S136.
Harris A C 1956 Regeneration of jarrah (Eucalyptus marginata). Australian Forestry 20,
54-62.
Heinrich I and Banks J C G 2005 Dendroclimatological potential of the Australian red
cedar. Australian Journal of Botany 53, 21-32.
Jama B, Buresh R J, Ndufa J K and Shepherd K D 1998 Vertical distribution of roots and
soil nitrate: tree species and phosphorus effects. Soil Science Society of America
Journal 62, 280-286.
Kew G A, Mengler F C and Gilkes R J 2007 Regolith strength, water retention and
implications for ripping and plant root growth in bauxite mine restoration.
Restoration Ecology 15, (Supplement) S54-S64.
Koch J M 2007 Alcoa's mining and restoration process in south Western Australia.
Restoration Ecology 15, (Supplement) S11-S16.
Koch J M and Samsa G P 2007 Restoring Jarrah Forest trees after bauxite mining in
Western Australia. Restoration Ecology 15, (Supplement) S17-S25.
Koch J M and Ward S C 2005 Thirteen-year growth of jarrah (Eucalyptus marginata) on
rehabilitated bauxite mines in south-western Australia. Australian Forestry 68, 176-
185.
106
Koch J M, Ward S C, Grant C D and Ainsworth G L 1996 Effects of bauxite mine
restoration operations on topsoil seed reserves in the jarrah forest of Western
Australia. Restoration Ecology 4, 368-376.
Lambers H and Poorter H 1992 Inherent variation in growth rate between higher plants: A
search for physiological causes and ecological consequences. Advances in
Ecological Research 23, 187-261.
Leal S, Pereira H, Grabner M and Wimmer R 2004 Tree-ring structure and climatic effects
in young Eucalyptus globulus Labill. grown at two Portuguese sites: preliminary
results. Dendrochronologia 21, 139-146.
Macfarlane C and Adams M A 1998 δ13C of wood in growth-rings indicates cambial
activity of drought-stressed trees of Eucalyptus globulus. Functional Ecology 12,
655-664.
McArthur W M 1991 Reference Soils of South-Western Australia. Department of
Agriculture, Western Australia, Perth.
Mickovski S B and Ennos A R 2002 A morphological and mechanical study of the root
systems of suppressed crown Scots pine Pinus sylvestris. Trees 16, 274-280.
Morrow P A and LaMarche V C, Jr. 1978 Tree-ring evidennce for chronic insect
suppression in subalpine Eucalyptus. Science 201, 1244-1246.
Nicholls J W P 1974 Effect of prescribed burning in a forest on wood characteristics of
jarrah. Australian Forestry 36, 178-189.
O'Grady A P, Worledge D and Battaglia M 2005 Temporal and spatial changes in fine root
distributions in a young Eucalyptus globulus stand in southern Tasmania. Forest
Ecology and Management 214, 373-383.
Ogden J 1978 On the dendrochronological potential of Australian trees. Australian Journal
of Ecology 3, 339-356.
Pate J and Arthur D 1998 δ13C analysis of phloem sap carbon: novel means of evaluating
seasonal water stress and interpreting carbon isotope signatures of foliage and trunk
wood of Eucalyptus globulus. Oecologia 117, 301-311.
Rayner M E 1991 Site index and dominant height growth curves for regrowth karri
(Eucalyptus diversicolor F. Muell.) in south-western Australia. Forest Ecology and
Management 44, 261-283.
107
Readshaw J L and Mazanec Z 1968 Use of growth rings to determine past phasmatid
defoliations of alpine ash forests. Australian Forestry 32, 29-36.
Sadlier S B and Gilkes R J 1976 Development of bauxite in relation to parent material near
Jarrahdale, Western Australia. Journal of the Geological Society of Australia 23,
333-334.
Schulze E D, Turner N C, Nicolle D and Schumacher J 2006 Leaf and wood carbon isotope
ratios, specific leaf areas and wood growth of Eucalyptus species across a rainfall
gradient in Australia. Tree Physiology 26, 479-492.
Shea S R, Hatch A B, Havel J J and Ritson P 1975 The effect of changes on forest structure
and composition on water quality and yield from the northern jarrah forest. In
Managing Terrestrial Ecosystems. Eds. J Kikkawa and H A Nix. Proceedings of the
Ecological Society of Australia.
Skomarkova M V, Vaganov E A, Mund M, Knohl A, Linke P, Boerner A and Schulze E D
2006 Inter-annual and seasonal variability of radial growth, wood density and
carbon isotope ratios in tree rings of beech (Fagus sylvatica) growing in Germany
and Italy. Trees 20, 571-586.
Spoor G and Godwin R J 1978 An experimental investigation into the deep loosening of
soil by rigid tines. Journal of Agricultural Engineering Research 23, 243-258.
Stahle D W, Mushove P T, Cleaveland M K, Roig F and Haynes G A 1999 Management
implications of annual growth rings in Pterocarpus angolensis from Zimbabwe.
Forest Ecology and Management 124, 217-229.
Stoneman G L, Bradshaw F J and Christensen P 1989 Silviculture. In The jarrah forest: a
complex Mediterranean ecosystem. Eds. B Dell, J J Havel and N Malajczuk. pp
335-355. Kluwer Academic Publishers, Dordrecht.
Stoneman G L and Dell B 1993 Growth of Eucalyptus marginata (jarrah) seedlings in a
greenhouse in response to shade and soil temperature. Tree Physiology 13, 239-252.
Stoneman G L, Dell B and Turner N C 1995 Growth of Eucalyptus marginata (jarrah)
seedlings in Mediterranean-climate forest in south-west Australia in response to
overstorey, site and fertiliser application. Forest Ecology and Management 79, 173-
184.
108
Stoneman G L, Turner N C and Dell B 1994 Leaf growth, photosynthesis and tissue water
relations of greenhouse-grown Eucalyptus marginata seedlings in response to water
deficits. Tree Physiology 14, 633-646.
Stoneman G L and Whitford K 1995 Analysis of the concept of growth efficiency in
Eucalyptus marginata (jarrah) in relation to thinning, fertilising and tree
characteristics. Forest Ecology and Management 76, 47-53.
Szota C, Veneklaas E J, Koch J M and Lambers H 2007 Root architecture of jarrah
(Eucalyptus marginata) trees in relation to post-mining deep ripping in Western
Australia. Restoration Ecology 15, (Supplement) S65-S73.
Todd M C L, Grierson P F and Adams M A 2000 Litter cover as an index of nitrogen
availability in rehabilitated mine sites. Australian Journal of Soil Research 38, 423-
433.
Trouet V 2006 Annual growth ring patterns in Brachystegia spiciformis reveal influence of
precipitation on tree growth. Biotropica 38, 375-382.
Ward S C 2000 Soil development on rehabilitated bauxite mines in south-west Australia.
Australian Journal of Soil Research 38, 453-464.
Ward S C and Koch J M 1995 Early growth of jarrah (Eucalyptus marginata Donn ex
Smith) on rehabilitated bauxite minesites in south-west Australia. Australian
Forestry 58, 65-71.
Ward S C and Koch J M 1996 Biomass and nutrient distribution in a 15.5 year old forest
growing on a rehabilitated bauxite mine. Australian Journal of Ecology 21, 309-
315.
Warren C R, Bleby T M and Adams M A 2007 Changes in gas exchange versus leaf solutes
as a means to cope with summer drought in Eucalyptus marginata. Oecologia 154,
1-10.
Whitford K R 2002 Hollows in jarrah (Eucalyptus marginata) and marri (Corymbia
calophylla) trees. I. Hollow sizes, tree attributes and ages. Forest Ecology and
Management 160, 201-214.
Wills A J, Burbidge T E and Abbott I 2004 Impact of repeated defoliation on jarrah
(Eucalyptus marginata) saplings. Australian Forestry 67, 194-198.
109
Concluding Discussion
Major Findings
To meet the global demand for mineral resources, it is likely that mining activities will
expand into previously undisturbed native vegetation. Mine-restoration techniques
must therefore ensure that post-mining landscapes can support the flora, fauna,
processes and cycles of unmined vegetation. With any mining activity, disturbance of
the soil profile is the major process, which has the potential to threaten the long-term
survival of restored vegetation, in particular, species which rely on access to large soil
volumes throughout the profile. Jarrah (Eucalyptus marginata) is one such species,
which requires access to soil moisture at depth in order to survive periods of drought in
the Mediterranean climate of south-western Australia.
This thesis aimed to determine whether soil constraints were responsible for
poor tree growth at low-quality restored bauxite mine sites in the jarrah forest of south-
western Australia. If soil constraints are common throughout the restored landscape, it
is important to assess the response of tree species in order to determine their capacity
for long-term growth and survival. The present study therefore examined root-system
morphologies to determine how they changed in response to soil constraints. When soil
constraints limit the ability of plants to access water resources, their capacity to
maintain water status during periods of drought can be diminished. This thesis
therefore examined seasonal physiological patterns of the two major tree species at
restored sites, jarrah and marri (Corymbia calophylla), in relation to soil constraints, to
determine whether they exacerbate water stress during drought, and also to identify any
differences in drought-response between the two species. Studies of root-system
morphology present a snapshot in time of the response to soil constraints, while
physiological studies present a short-term seasonal response. In order to describe long-
term responses to soil constraints, the pattern of development of jarrah since
establishment was examined over time.
The present study contains the first report of root system morphologies of jarrah
at restored bauxite mine sites (Chapter 1). Restriction of coarse roots to the top 0.5 m of
the soil profile was associated with reduced tree and stand productivity, indicating that
above-ground productivity is directly related to root system development (Chapter 1).
As a result of mining-related compaction, subsoil access by roots at restored sites was
110
restricted to riplines, indicating that deep-ripping is an operation critical to the success
of vegetation at restored bauxite mines. Trees developed different root system
morphologies depending on their immediate soil conditions (Chapter 1). Trees that
accessed riplines with their taproot had greater girth and height than those that accessed
riplines with a large sinker root that originated from a large lateral root, which may
indicate resources available for above-ground growth are greater if the taproot is able to
penetrate the subsoil. An alternative explanation is that access to subsoil via a sinker
root takes longer than access via the taproot, thus the smaller size of these trees may be
a result of a growth lag, a theory supported by tree-ring analysis results (Chapter 3). At
the site with shallow soil, trees produced a large number of sinker roots, presumably a
result of failure of the primary root system to penetrate the subsoil, thus triggering the
development of more sinker roots along the length of the lateral root. This regular
pattern of root development in response to soil conditions may explain how jarrah trees
can produce a wide range of root system morphologies (Kimber 1974) and survive a
wide range of natural (Brooker and Kleinig 2001) and disturbed soil profiles (Kew et al.
2007).
Jarrah and marri trees at low-quality sites with restricted root systems
experienced increased water stress and decreased photosynthetic gas exchange,
compared to trees at high-quality sites (Chapter 2). This may explain the observed
slower growth rates and smaller stature of the trees at the low-quality site (Chapters 2
and 3). Trees at the high-quality site showed lower midday water potentials during leaf
expansion which suggests that competition, i.e. the high number of stems per hectare,
was too high and that a reduction in the number of stems may reduce pressure on water
resources. With regard to differences between the two species, jarrah achieved higher
rates of photosynthesis and lower leaf water status (midday leaf water potential and
average daily leaf relative water content) during drought compared to marri, which
indicates that leaves of jarrah have a higher desiccation tolerance than those of marri,
and may explain faster growth rates of jarrah trees (Chapter 2). The higher
photosynthesis and stomatal conductance at lower water status of jarrah was associated
with elastic adjustment of cell walls during drought. The fact that marri maintains
lower stomatal conductance (and therefore loses less water) and maintains a higher
water status (midday leaf water potential and average daily leaf relative water content)
during drought suggests that it is a more conservative water user than jarrah, and that it
may be better suited to surviving extended periods of drought. No coarse roots were
111
found in the subsoil at the low quality site; therefore it is unlikely that marri maintained
a higher water status through superior access to soil moisture. It is also unlikely that
marri maintained higher water status through enhanced stomatal sensitivity to high
vapour pressure deficits and/or declining soil water status, as there was no consistent
difference between stomatal sensitivity of the two species. Leaves of marri osmotically
adjusted during drought, which may explain their ability to maintain a higher water
status compared with jarrah. Although osmotic adjustment in jarrah was shown in a
glasshouse trial where seedlings were exposed to a rapidly developing drought
(Stoneman et al. 1994), it has not been demonstrated by saplings in the field (Bleby
2003; Warren et al. 2007). The present study found no osmotic adjustment in jarrah,
however, the identification of an increase in tissue elasticity in response to drought,
represents the discovery of a previously unknown physiological drought-response in the
species. Osmotic adjustment and the high cell-wall elasticity of marri leaves during
drought are also novel findings. The work presented here therefore presents a
significant contribution to our knowledge of contrasting ecophysiological mechanisms
underlying drought response in these two co-occurring eucalypts.
Studies of root system morphology and short-term leaf-scale physiology
represent a snapshot of the response of trees to stress. To describe at what stage stress
began to effect tree growth, Chapter 3 used the novel approach of using tree-ring
analysis to describe above-ground growth patterns of jarrah over time at the two
contrasting restored bauxite mine sites. Tree-ring analysis has typically been applied in
studies of tree growth in relation to long-term environmental factors (such as climate);
however, the application of the technique here has proven extremely useful. Tree-ring
analysis in the present study showed that trees growing on shallow soil showed slow
rates of growth from the first year onwards (Chapter 3), which may indicate that
restriction of the primary root system (Chapter 1) reduced above-ground productivity
early in the life of the tree. Trees unable to access friable soil in a ripline with their
taproot (trees situated on crests) showed slow initial development prior to a boost in
growth. This delayed boost in growth was probably due to the additional time taken for
the lateral roots to grow and produce sinker roots. Trees which could access subsoil in a
more direct way with their taproots showed rapid initial growth which then declined
over time, giving them a head start over trees without taproots. Growth of trees at sites
with low soil moisture-storage capacity was more responsive to rainfall received during
the previous summer and current autumn (prior to the diameter growth phase), whereas
112
growth of trees at sites with a higher capacity to store soil moisture was more dependent
on rainfall received during the current autumn and spring (during the diameter growth
phase).
These results clearly demonstrate that impenetrable subsoils, if not adequately
ripped, can limit the productivity of tree species at restored bauxite mine sites.
Implications for mine-site restoration
Three key findings from this thesis have the potential to influence or change current
bauxite mine restoration practices:
1. the strong link between soil conditions, deep-ripping and tree productivity;
2. desiccation tolerance of jarrah versus desiccation avoidance and water
conservation of marri; and
3. the relationship between root morphology and stand development over time.
Although the chapters in this thesis examined different aspects of trees at
restored sites, the primary factor driving all results was soil depth. Shallow soil limited
root development, causing a decline in water status and restriction of photosynthesis
earlier in the growing season, limiting annual increases in diameter growth which
resulted in lower tree productivity. The key implication for restoration here is therefore
to continue to improve methods of soil profile construction to ensure that the vegetation
is able to achieve adequate root depth.
Marri has received relatively little attention compared with jarrah in previous
studies, and reported differences in water status during drought (Colquhoun et al. 1984)
have never been studied in detail. The findings of this thesis highlight the importance
of marri as a significant component of the jarrah forest, as it clearly demonstrates
different drought-response mechanisms when compared with jarrah. Marri has a greater
potential to survive sites where water availability is predicted to be low or highly
variable as it uses water more conservatively than jarrah does. Aside from the increased
potential to survive extended periods of drought, there are several other reasons why
marri should be restored at higher frequencies in certain areas. Members of the
Corymbia genus are typically better able to capture sparingly soluble nutrients and have
higher inherent resistance to pests and diseases (Florence 1996). Furthermore, as the
value of marri as a timber resource has significantly increased in recent years, a higher
proportion of marri trees will enrich the forest resource.
113
Over-stocked restored stands established during the 1990’s are already being
actively thinned to decrease competition and increase growth of retained stems (Grant et
al. 2007). Evidence presented in this thesis indicates that trees on crests rather than
riplines should be preferentially thinned since they have lower growth potential and
abnormal root systems. Trees in riplines were larger than those on crests, presumably a
result of direct access to subsoil. Consequently these trees are likely to demonstrate a
greater growth response after thinning (Florence 1996). Therefore, if forest productivity
targets are not being met, selectively thinning trees on crests and retaining trees in
riplines is more likely to achieve the desired outcome. Also, as trees on crests were
shown to have no significant taproot and only 1-3 lateral roots for support; they are
more likely to be susceptible to windthrow (Coutts 1983; Mickovski and Ennos 2002).
Trees in riplines are also at an advantage nutritionally, as leaf litter and therefore
nutrients tend to concentrate in riplines (Todd et al. 2000; Ward 2000). On the other
hand, non-selective tree thinning is more likely to increase the diversity of the canopy
and broaden the size class distribution of the stand (Florence 1996), making it more
closely resemble an unmined forest (Abbott and Loneragan 1983; Abbott 1984).
Study limitations and future research
The limitations of this study, particularly relating to the use of only two field sites, are
acknowledged. Nevertheless, the present approach has given a more thorough
understanding of the whole-tree mechanisms and growth strategies of trees at restored
bauxite mine sites. Glasshouse studies are often used to identify the nature and
magnitude of the response of a species to limiting factors such as water or nutrient
deficits. However, where the target species is a tree, it is dangerous to assume that
seedling response to stress in the glasshouse will be similar to the response of a sapling
or tree in the field, where it has been able to develop in response to the stress over time.
Therefore, in this study, field studies were preferable when identifying factors limiting
tree development on restored bauxite mine sites. Unfortunately, field studies are limited
in their ability to manipulate variables and apply treatments in order to describe the
response of a species. This thesis has used the approach of comparing field sites with
obvious differences in tree size and densities to investigate causes of poor growth at
restored sites.
In this study poor growth of jarrah within restored sites was related to poor root
growth. Excavation of twelve root systems by hand (to prevent damage) in the lateritic
114
soils of the northern jarrah forest was a major undertaking, taking one person five
months to complete due to the hardness of the soil material. Consequently the
experimental design had obvious limitations in terms of the number of replicates (three
per site and situation) and the number of species (jarrah only). However despite these
limitations the study significantly contributed to our knowledge of jarrah root systems
and to the determination of restoration success. Describing tree root systems in these
conditions was difficult; however, I would encourage fellow researchers to continue this
line of research and, in particular, to explore differences in root system morphology and
physiology between jarrah and marri, and indeed between any co-occurring species. In
this thesis, differences in root system morphology in response to deep ripping was a
higher priority than describing differences between species, which unfortunately forced
a decision between comparing species or situations. Studies of contrasting survival
mechanisms of co-occurring eucalypts are increasing along with the need to predict the
response of vegetation types to altered environments, such as mined landscapes and new
climatic conditions (Merchant et al. 2006).
This thesis has shown significant physiological differences between co-
occurring eucalypts at restored sites. The next step is to further investigate the
differences in jarrah and marri that may improve their deployment in restoration and
management in forestry. Recent studies have utilised osmolytes as a screening tool for
drought tolerance mechanisms in eucalypts (Merchant et al. 2006; Merchant et al. 2007;
Arndt et al. 2008). Given the differences in elastic and osmotic adjustments between
jarrah and marri presented here (Chapter 2), a large-scale paired sampling of the two
species across rainfall and soil gradients has the potential to determine how, and under
what circumstances, jarrah and marri display elastic or osmotic adjustment.
Furthermore, to explain the higher water status of marri compared to jarrah during
drought, comparative studies of levels of leaf ABA (Davies et al. 1990; Tardieu and
Davies 1992) may assist with determining the underlying mechanism.
The present study has shown that root morphology (Chapter 1) and above-
ground growth rates (Chapter 3) differ between trees situated on crests and in riplines.
These results have potential implications for improved stand management, namely
stocking rates and thinning operations. Consequently, thinning trials based on these
findings, including preferential thinning of crest-situated trees, would be extremely
worthwhile.
115
The results presented here allow a synthesis of how the two restored sites
studied in this thesis will perform over time. In the long term, given the high water
stress experienced by trees at the low-quality site, drought-related mortality rates are
likely to increase, a result that cannot be altered by practical management actions. The
drought-avoiding/water-conserving physiology of marri when compared with jarrah is
likely to result in higher mortality of jarrah compared with marri at the low-quality site.
The high stocking rate at the high-quality site is likely to restrict tree growth rates in the
future. Trees situated in riplines are likely to continue to out-perform trees on crests, be
it due to their more direct access to the subsoil, or the result of having accessed the
subsoil and achieved maximum growth rates earlier than did trees on crests. In this
case, management in the form of thinning is highly likely to improve the growth of
retained trees and promote maturation of the stand.
References
Abbott I 1984 Comparisons of spatial pattern, structure, and tree composition between
virgin and cut-over jarrah forest in Western Australia. Forest Ecology and
Management 9, 101-126.
Abbott I and Loneragan O 1983 Response of jarrah (Eucalyptus marginata) regrowth to
thinning. Australian Forest Research 13, 217-229.
Arndt S K, Livesley S J, Merchant A, Bleby T M and Grierson P F 2008 Quercitol and
osmotic adaptation of field-grown Eucalyptus under seasonal drought stress.
Plant, Cell and Environment 31, 915-924.
Bleby T M 2003 Water use, ecophysiology and hydraulic architecture of Eucalyptus
marginata (jarrah) growing on mine rehabilitation sites in the jarrah forest of
south-western Australia. PhD Thesis, The University of Western Australia,
Perth.
Brooker M I H and Kleinig D A 2001 Field guide to eucalypts. Vol. 2, South-western
and southern Australia. Bloomings Books, Melbourne. pp. 428.
Colquhoun I J, Ridge R W, Bell D T, Loneragan W A and Kuo J 1984 Comparative
studies in selected species of Eucalyptus used in rehabilitation of the northern
jarrah forest, Western Australia. I. Patterns of xylem pressure potential and
diffusive resistance of leaves. Australian Journal of Botany 32, 367-373.
Coutts M P 1983 Root architecture and tree stability. Plant and Soil 71, 171-188.
116
Davies W J, Mansfield T A and Hetherington A M 1990 Sensing of soil water status
and the regulation of plant growth and development. Plant, Cell and
Environment 13, 709-719.
Florence R G 1996 Ecology and silviculture of eucalypt forests. CSIRO Publishing,
Melbourne. pp. 413.
Grant C D, Norman M A and Smith M A 2007 Fire and silvicultural management of
restored bauxite mines in Western Australia. Restoration Ecology 15,
(Supplement) S127-S136.
Kew G A, Mengler F C and Gilkes R J 2007 Regolith strength, water retention and
implications for ripping and plant root growth in bauxite mine restoration.
Restoration Ecology 15, (Supplement) S54-S64.
Kimber P C 1974 The root system of jarrah (Eucalyptus marginata). pp 1-5. Forests
Department of Western Australia, Perth.
Merchant A, Callister A, Arndt S, Tausz M and Adams M 2007 Contrasting
physiological responses of six Eucalyptus species to water deficit. Annals of
Botany 100, 1507-1515.
Merchant A, Tausz M, Arndt S K and Adams M A 2006 Cyclitols and carbohydrates in
leaves and roots of 13 Eucalyptus species suggest contrasting physiological
responses to water deficit. Plant, Cell and Environment 29, 2017-2029.
Mickovski S B and Ennos A R 2002 A morphological and mechanical study of the root
systems of suppressed crown Scots pine Pinus sylvestris. Trees 16, 274-280.
Stoneman G L, Turner N C and Dell B 1994 Leaf growth, photosynthesis and tissue
water relations of greenhouse-grown Eucalyptus marginata seedlings in
response to water deficits. Tree Physiology 14, 633-646.
Tardieu F and Davies W J 1992 Stomatal response to ABA is a function of current plant
water status. Plant Physiology 98, 540-545.
Todd M C L, Grierson P F and Adams M A 2000 Litter cover as an index of nitrogen
availability in rehabilitated mine sites. Australian Journal of Soil Research 38,
423-433.
Ward S C 2000 Soil development on rehabilitated bauxite mines in south-west
Australia. Australian Journal of Soil Research 38, 453-464.
Warren C R, Bleby T M and Adams M A 2007 Changes in gas exchange versus leaf
solutes as a means to cope with summer drought in Eucalyptus marginata.
Oecologia 154, 1-10.