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

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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

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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.

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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

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Churchward H M and Dimmock G M 1989 The soils and landforms of the northern jarrah

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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.

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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.

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landscapes developing secondary salinity using the ventilated-chamber technique.

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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

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Inc., New York.

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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.

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Koch J M 2007 Alcoa's mining and restoration process in south Western Australia.

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Koch J M and Samsa G P 2007 Restoring Jarrah Forest trees after bauxite mining in

Western Australia. Restoration Ecology 15, (Supplement) S17-S25.

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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.

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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.

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relation to soil strength arising from compaction. Plant and Soil 182, 1-11.

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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.

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subsoil on root development, water uptake and growth of radiata pine. Tree

Physiology 10, 297-306.

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related to species abundance? A congeneric comparison between rare and common

species in the south-western Australian flora. Journal of Ecology 91, 58-67.

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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.

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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

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unfavourable physical conditions? A model-based hypothesis. Plant and Soil 217,

151-157.

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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

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N D J F M A M J J A S O N D J F M

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m)

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)

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Tem

pera

ture

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)0

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N D J F M A M J J A S O N D J F M

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D (k

Pa)

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2003 2004 2005

B

0

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100

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N D J F M A M J J A S O N D J F M

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)0

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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.

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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).

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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

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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

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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.

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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

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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.

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