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Annals of Botany 108: 347 –357, 2011
doi:10.1093/aob/mcr135, available online at www.aob.oxfordjournals.org
Pushed to the limit: consequences of climate change for the Araucariaceae:
a relictual rain forest family
Catherine A. Offord*
The Australian Botanic Garden, Mount Annan, Royal Botanic Gardens and Domain Trust, Mount Annan Drive, Mount Annan,
NSW 2567, Australia
* E-mail [email protected]
Received: 4 January 2011 Returned for revision: 18 February 2011 Accepted: 11 April 2011 Published electronically: 3 July 2011
† Background and Aims Under predicted climate change scenarios, increased temperatures are likely to predispose trees to leaf and other tissue damage, resulting in plant death and contraction of already narrow distribution
ranges in many relictual species. The effects of predicted upward temperatures may be further exacerbated by
changes in rainfall patterns and damage caused by frosts on trees that have been insufficiently cold-hardened.
The Araucariaceae is a relictual family and the seven species found in Australia have limited natural distributions
characterized by low frost intensity and frequency, and warm summer temperatures. The temperature limits for
these species were determined in order to help understand how such species will fare in a changing climate.
† Methods Experiments were conducted using samples from representative trees of the Araucariaceae species
occurring in Australia, Agathis (A. atropurpurea, A. microstachya and A. robusta), Arauacaria (A. bidwilli,
A. cunninghamii and A. heterophylla) and Wollemia nobilis. Samples were collected from plants grown in a
common garden environment. Lower and higher temperature limits were determined by subjecting detached
winter-hardened leaves to temperatures from 0 to –17 8C and summer-exposed leaves to 25 to 63 8C, then
measuring the efficiency of photosystem II (Fv/Fm) and visually rating leaf damage. The exotherm, a sharp
rise in temperature indicating the point of ice nucleation within the cells of the leaf, was measured on detached
leaves of winter-hardened and summer temperature-exposed leaves.
† Key Results Lower temperature limits (indicated by FT50, the temperature at which PSII efficiency is 50 %, and
LT50 the temperature at which 50 % visual leaf damage occurred) were approx. – 5.5 to –7.5 8C for
A. atropurpurea, A. microstachya and A. heterophylla, approx. –7 to –9 8C for A. robusta, A. bidwillii and
A. cunninghamii, and –10.5 to –11 8C for W. nobilis. High temperature damage began at 47.5 8C for
W. nobilis, and occurred in the range 48.5– 52 8C for A. bidwillii and A. cunninghamii, and in the range
50.5–53.5 8C for A. robusta, A. microstachya and A. heterophylla. Winter-hardened leaves had ice nucleation
temperatures of – 5.5 8C or lower, with W. nobilis the lowest at –6.8 8C. All species had significantly higher
ice nucleation temperatures in summer, with A. atropurpurea and A. heterophylla forming ice in the leaf at temperatures .3 8C higher in summer than in winter. Wollemia nobilis had lower FT50 and LT50 values than its ice
nucleation temperature, indicating that the species has a degree of ice tolerance.
† Conclusions While lower temperature limits in the Australian Araucariaceae are generally unlikely to affect
their survival in wild populations during normal winters, unseasonal frosts may have devastating effects on
tree survival. Extreme high temperatures are not common in the areas of natural occurrence, but upward temperature shifts, in combination with localized radiant heating, may increase the heat experienced within a canopy
by at least 10 8C and impact on tree survival, and may contribute to range contraction. Heat stress may explain
why many landscape plantings of W. nobilis have failed in hotter areas of Australia.
Key words: Hardiness, frost, high temperature, climate change, Araucariaceae, rain forest.
IN T RO DU C T IO N
With a predicted warming trend over the Earth’s surface, many
plant species face an uncertain future. Climate projections for
Eastern Australia based on the effects of atmospheric greenhouse gases of anthropogenic origin remaining at current or at
increased levels indicate a substantial upward shift in temperature ranges (CSIRO, 2010). Coupled with changes in rainfall
frequency and intensity, temperature shifts are likely to impact
on plant growth and survival, and a high degree of regional variation is expected (IPCC, 2007). There is concern for Australian
wet-tropical and sub-tropical forest taxa with restricted distributions that are already fragmented through past climate shifts.
Such species should be considered for proactive management,
given greater information on their vulnerability to climate
change and response to proposed actions (Hilbert, 2007).
Species of greatest concern are those that have narrow geographical ranges that will become dissociated from their presentday temperature envelopes, especially those species with a
North – South range of ,300 km or an elevation range
,300 m (Westoby and Burgman, 2006).
The Araucariaceae is an evergreen conifer family from
temperate, tropical and sub-tropical regions of the Southern
Hemisphere, although they once ranged into the Northern
Hemisphere (Stockey, 1982). They are emergent rain forest
species that once occupied vast distribution ranges, peaking in
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* Boland et al. (2006).
†
Australian Bureau of Meteorology.
‡
From data recorded at one site 1998– 2006.
42.2 8C; –8.3 8C; 0.3 d; 38.4 d (Mudgee)†;
35.9 8C; – 8.2 8C; 0 d; 17.3 d (Nullo)†;
34.9 8C; –1.8 8C‡
0– 1/24– 26 8C; moderate to high frost
incidence†
900 m
Norfolk Island
pine
Wollemi pine
Araucaria heterophylla (Salisb.) Franco (cultivated source,
29 8,167 8, 30 m)
Wollemia nobilis W.G.Jones, K.D.Hill, J.M.Allen (950218,
32 8S, 149 8E, 900 m)
18– 19/23 –2 8C; no frost†
Hoop pine
Araucaria cunninghamii Aiton ex A.Cunn (932671, 28 8S,
153 8E, 30 m)
0 –300 m
5– 10/28 –32 8C; low to moderate frost
(up to 30 p.a.)*
South: 1– 7/27– 30 8C; North: 16– 33 8C;
low to moderate frost incidence*
150– 1200 m
0 –1000 m
44.2 8C; –2.8 8C; 0 d; 0.3 d (Tewantin)†;
36.7 8C; – 0.6 8C; 0 d; 0.3 d (Atherton)†
41.7 8C; –6.2 8C; 1.1 d; 19.3 d (Dalby)†;
41.2 8C; –4 8C; 0.2 d; 0.3 d (Imbil)†
36 8C; – 3.5 8C; 0 d; 7.7 d (Dorrigo)†; 37.7 8C;
0.8 8C; 0 d; 0 d (Bundaberg)†; 40.6 8C; 7 8C;
0 d; 0 d (Coen)†
28.4 8C; 6.2 8C; 0 d; 0 d (Norfolk Aero)†
13– 19/30 –32 8C; low frost incidence*
0 –900 m
Queensland
Kauri
Bunya pine
36.7 8C; –0.6 8C; 0 d; 0.3 d (Atherton)†
10/30 8C; low to moderate frost incidence*
600– 1000 m
Bull Kauri
38.1 8C; –5 8 C; 0 d; 1.6 d (Herberton)†
900– 1500 m
Blue Kauri
Agathis atropurpurea B.Hyland (971022, 17 8S, 145 8E,
1,140 m)
Agathis microstachya Bailey and C.T.White (20010050,
17 827’S, 145 8 38’E, 740 m)
Agathis robusta (F. Muell.) Bailey (86429, 25 8S, 153 8E,
10 m)
Araucaria bidwilli Hook. (960623, 26 8S, 151 8E, 1100 m)
10/30 8C; low to moderate frost incidence*
Temperature range (min/max monthly
average); frost
Altitude range
Common name
Species (accession, lat, long, alt of provenance)
diversity in the Jurassic and declining towards the end of the
Cretaceous (Miller, 1977). Perhaps as late as 140 000 years
ago, the Araucarian forests were still a significant component
of the Australian vegetation (Kershaw, 1994). With the drying
and increased variability of the climate of the Australian
continent, ranges contracted significantly so that by the late
Pliocene, the Araucarian forests in south-eastern Australia
were replaced by a mosaic of sclerophyllous forests and open
vegetation, and localized cool temperate rain forests
(Gallagher et al., 2003). By the late Pleistocene, Araucaria
extinctions or range contractions had occurred in north-eastern
Australia (Kershaw, 1994). Several species are severely
restricted in distribution, especially Wollemia nobilis of which
,100 trees grow in the wild, and Araucaria heterophylla,
found naturally only on Norfolk and Phillip Islands. Agathis
atropurpurea and Agathis microstachya are also very limited
in distribution. Agathis robusta, Araucaria cunninghamii and
Arauacaria bidwilli are relatively more widely distributed and
are found from sea level to high altitude (Table 1).
Low temperatures are thought to determine the latitudinal and
altitudinal limits of woody plants (Larcher, 2005) including
Australian rain forest species (Dodson and Myers, 1986).
Episodic, low temperature events, such as frosts, are more
likely to influence plant distributions than average minimum
air temperatures (Loik et al., 2004). Under climate change,
frosts are likely to be more frequent in some areas and less frequent in others (Inouye 2000). The impacts of frost range from
cellular to ecosystem in scale (Saxe et al., 2001; Loik et al.,
2004). Ice can enter the leaf through stomata or hydathodes, or
freezing nucleation of intrinsic water can occur (Pearce, 2001).
Within a leaf, freezing occurs as a wave, and ice may travel at
3 – 47 mm s21, originating in the xylem vessels and tracheids
(Hacker and Neuner, 2007) of the mid-vein, and spreading
rapidly into the leaf (Ball et al., 2002). The freezing of apoplastic
water in the leaf is generally characterized by a sharp increase in
temperature known as the exotherm – the release of latent heat –
with slow recovery to lower temperatures. The length of recovery is related to the position of freezing in the leaf, i.e. the leaf
margin – quicker – and near the mid-vein – more slowly.
Frost, resulting in the formation of ice crystals in plant
tissue, may lead to plant death, or may at least reduce the functioning of sensitive plant parts such as buds, ovaries and
leaves. Plants may therefore be killed outright or become
predisposed to insect or fungal attack leading to plant death
(Inouye, 2000).
Structural differences between acclimated and nonacclimated leaves have been documented. In Eucalytus pauciflora, for example, tissue death is caused by the formation of
intracellular ice in the cambium and phloem, with dehydration
of cells generally leading to irreversible tissue damage. In contrast, acclimated leaves are characterized by the formation of
extracellular ice in expansion zones in the mid-vein, resulting,
largely, in restoration of the original functions of the leaves on
thawing (Ball et al., 2004). Leaf death may retard plant
growth/regrowth, and the ultimate effect of leaf death and
stem survival would need to be investigated in order to
determine fully the temperature limits of vulnerable species.
Araucariaceae species are generally considered to be tolerant of mild frost. Visual inspection of frozen plant parts of
Southern Hemisphere conifers for browning indicated that
Lowest and highest recorded temperatures at nearest
weather station(s); mean days .40 8C; and ,0 8C
Offord — Temperature limits for relictual rain forest Araucariaceae
TA B L E 1. Altitude, temperature and frost incidence in the natural range of Australian Araucariaceae species
348
Offord — Temperature limits for relictual rain forest Araucariaceae
A. bidwillii was the most frost resistant of the Araucariaceae
tested, with damage not occurring until – 10 8C for this
species, while damage occurred at – 7 8C for A. australis and
at – 5 8C for A. excelsa and A. cunninghamii, the least resistant
(Sakai et al., 1981).
High temperatures also limit plant growth and species distribution. The effects of high temperatures on plants are often
more complex than those caused by cold temperatures and
are, typically, photoinactivation (which may be reversible),
followed by irreversible destruction of the photosynthetic
apparatus, such as by disconnection of photosystem II (PSII)
reaction centres and biomembrane lesions (Berry and
Bjorkman, 1980) which is irreversible. Consequently,
measurements of heat damage, and cold damage for that
matter, should be made after reversible damage has been
repaired, usually after several days to 1 week (see, for
example, Krause et al., 2010).
In a study of Australian rain forest species, Cunningham and
Read (2006) found that seedlings of tropical species have a
greater heat tolerance (51– 55 8C) than temperate species
(48 – 51 8C), but considerably less tolerance than many semiarid sub-tropical woody plants (50 – 60 8C). These ranges represent the temperatures at which there was 50 % visible leaf
damage (LT50). They also found that the range of temperatures
within which all species tested maintained at least 50 % of
their initial photosynthetic efficiency were consistently in the
order of 56– 60 8C, regardless of their lower and upper limits.
Techniques used to determine the effects of temperature on
plant organs, include: visual assessment of damage (e.g. Sakai
et al., 1981; Deans et al., 1995), measurement of fluorescence
(e.g. Neuner and Buchner, 1999; Zhang et al., 2003) or electrical impedance (e.g. Zhang et al., 2010), and fractal analysis
(Mancuso et al., 2004). Electrolyte leakage, measured by relative conductivity, is one of the most widely used methods for
assessing low temperature effects as it is based on release of
35
30
349
cell contents due to cell wall hydrolysis and is easily measured
(see, for example, Sutinen et al., 1992; Strimbeck et al., 2007).
The ability to measure temperature tolerance adequately using
this technique is variable, however, and depends on the
species, the material used and the conditions of testing. It is,
therefore, often appropriate to use a number of techniques to
make assessments (Mancuso et al., 2004), especially when
comparing species that are not well characterized for
temperature tolerance.
Given the limited natural distributions of Australian
Araucariaceae and the increased need for knowledge of temperature limits to manage wild stands, forestry and horticultural
specimens, the temperature tolerance range of seven species
was investigated using plants from a common garden environment. Of particular interest was the question of whether highaltitude tropical species are more likely to be tolerant of high
temperatures, while being more sensitive to frost, than more
temperate species.
M AT E R I A L S A N D M E T H O D S
Plant material and site temperatures
Leaf samples were taken in late winter (21 August 2006) from
Araucariaceae species (Table 1) grown at The Australian
Botanic Garden, Mount Annan, NSW Australia (34 805’S,
150 847’E). All plants had been grown from seed, were sexually mature and were between 9 and 14 years old. During
winter 2006, the nearest weather station, Camden, recorded
21 separate frost events and several minimum night temperatures of – 4 8C in the months preceding the tests (Fig. 1).
Material from the same trees was collected on 16 February
2007 following peak summer temperature exposure. The
lowest temperature for Camden since recording commenced
No. days < 0º C 2006
No. days > 35º C 2006
Max 2006
Min 2006
Max since 1943
Min since 1943
Temperature (ºC)
25
20
15
10
5
0
Jan Feb Mar Apr May Jun
Jul Aug Sep Oct Nov Dec
Month
F I G . 1. Average monthly minimum and maximum temperatures in 2006 and since 1943, and number of events of daily minimum or maximum temperatures
below 0 8C or above 35 8C, for Camden NSW in 2006 (Australian Bureau of Meteorology).
350
Offord — Temperature limits for relictual rain forest Araucariaceae
in 1943 was –6 8C (12 July 2002) and the highest was 45 8C
(30 January 2003).
To test the difference between the nearest Bureau of
Meteorology (BoM) screen temperature and the air temperature within the plant canopy, Thermocron iButton temperature
loggers (OnSolution, Sydney, Australia) were placed on
several different trees of A. atropurpurea, with three replicates
located on the eastern and three on the western sides of the
trees. Temperatures were logged every 15 min for 13 d in
late February 2009. The radiant heat factor was determined
as the average difference between temperatures on the
eastern and western sides of the trees. This factor was then
used to estimate the upper screen temperature limits for each
species.
FvFm and visual rating
Leaf samples (detached moistened terminal branch sections,
150 mm in length) were harvested from three trees per species.
Samples (three samples per tree) were collected from the
eastern side of the tree at a height of 1.5 – 3 m above ground
level. They were stored overnight prior to use in sealed
plastic bags at 3 8C (winter collections) and at 21 8C
(summer collections) to dark adapt and re-oxidate.
Winter-hardened samples were lightly ‘sandwiched’ in the
resealable plastic bag and placed into a variable-controlled
temperature freezer (Engel 40, Engel Australia). The temperature was slowly lowered by 3 8C h21 to the target temperature,
and was held at that temperature for 2 h to ensure equilibration
of the temperature throughout the samples, before being slowly
raised back to room temperature. The target temperatures
ranged from 0 to – 17 8C in 2 or 3 8C increments. Sealed
plastic bags containing summer temperature-exposed samples
were placed in a water bath and exposed for 30 min to temperature treatments ranging from 25 to 63 8C in 3 8C increments.
All samples were then stored in the plastic bags at room temperature for 2 weeks. Chlorophyll fluorescence was measured
using a MINI-PAM photosynthetic yield analyser (Walz,
Germany). Yield (Fv/Fm) was calculated to determine PSII
damage after the treatments. A visual rating of damage was
made based on a scale of 0 (no visible damage) through to 5
(all leaves, stems and buds brown or necrotic). Both measurements were made 7 d after treatment, as more immediate
measurements give less reliable results (Cunningham and
Read, 2006; Buchner and Neuner, 2009).
Ice nucleation temperature
A thermocouple (Walz Ni-CrNi, diameter 100 mm) was
attached using Micropore tape (3M Company) to the abaxial
side of a moist detached leaf in the mid-laminal position.
The leaf was placed in a resealable plastic bag and placed
into a variable-controlled temperature freezer. The temperature
was slowly lowered by 3 8C h21 and the mid-lamina temperature was recorded every 10 s using a logging device. For
A. cunninghamii and A. heterophylla, the thermocouple loop
was placed around a leaf (‘needle’) and taped in place.
Exotherms (sharp rises in temperature, with a slow recovery
to the freezer temperature), which show the temperature of
ice nucleation within and between the cells of the leaf, were
observed and recorded for 9 – 12 leaves of each species.
Data analysis
Using the Fv/Fm and visual rating data, the temperatures at
which significant damage occurs, the FT50 (50 % reduction in
Fv/Fm of leaf ) and LT50 (50 % lethal damage to leaf ) were
estimated as the inflection point ( parameter C) of eqn (1):
Y = [A/1 + eB(x−C) ] + D
(1)
where Y ¼ Fv/Fm or visual rating, A ¼ range of values,
B ¼ slope at the temperature of inflection, C ¼ inflection
point, D ¼ minimum value.
The logistic regression curves were also used to estimate LTi
(temperature at which damage was initiated) and LT100 (temperature at which 100 % tissue damage occurred) to show the
range over which damage occurred to that species. Using
FT50 and LT50 values for the individual trees, the species
were compared by analysis of variance (ANOVA) and the
treatment means compared by least significant difference
(l.s.d.) using the Genstat (Lawes Agricultural Trust, 2007)
package. Tspan, the temperature tolerance range, was calculated
for each species by taking the difference between upper and
lower FT50 and LT50 values.
Exotherm data were analysed by ANOVA and treatment
means compared by l.s.d.
R E S U LT S
Leaf damage
The leaf damage variables, Fv/Fm and visual damage rating,
were significantly correlated for all species at both low
(Table 2) and high temperatures (not shown; P , 0.001). The
strong relationship is reflected in the agreement between the
LTi, LT100 and LT50 values (Fig. 2) for the respective species.
In the lower temperature range, leaf damage was initiated at
approx. – 7.5 to – 8 8C in W. nobilis, at – 6 to – 6.5 8C in
A. cunninghamii and at – 4 to – 5 8C (P , 0.05) in the other
species. Arauacaria heterophylla was the only species to show
some difference between FTi and LTi (–5.5 and – 3.5 8C,
respectively), which may be the result of difficulty in measuring
fluorescence on the needles of this species. The visual rating is
TA B L E 2. Correlations between FT50 and LT50
temperature values (R 2 values)
Species
Agathis atropurpurea
Agathis microstachys
Agathis robusta
Araucaria bidwillii
Araucaria cunninghamii
Araucaria heterophylla
Wollemia nobilis
*** P , 0.001.
for
low
R2
0.90***
0.84***
0.70***
0.82***
0.82***
0.80***
0.76***
Offord — Temperature limits for relictual rain forest Araucariaceae
351
Upper temperature (ºC)
60
55
50
45
Wollemia
nobilis
Araucaria
heterophylla
Araucaria
cunninghamii
Araucaria
bidwillii
Agathis
robusta
Agathis
microstachya
Agathis
atropurpurea
Wollemia
nobilis
Araucaria
heterophylla
Araucaria
cunninghamii
Araucaria
bidwillii
LTi
LT50
LT100
Agathis
robusta
FTi
FT50
FT100
Agathis
microstachya
0
–2
–4
–6
–8
–10
–12
–14
–16
–18
–20
–22
Agathis
atropurpurea
Lower temperature (ºC)
40
F I G . 2. Ranges within which leaf damage occurs to Australian Araucariaceae species at low and high temperatures (+s.e.). FTi, FT50 and FT100 are the temperatures at which initial, 50 % and 100 % reduction in Fv/Fm occurred; LTi, LT50 and LT100 are the temperatures at which initial, 50 % and 100 % lethal leaf
damage occurred.
likely to be a more accurate measure of leaf damage in this
species. Maximum estimated damage occurred at – 12.5 to
– 14 8C in W. nobilis, at – 10 to – 11 8C in A. cunninghamii
and somewhere between – 7.5 and – 12 8C for the other
species. Again, A. heterophylla was damaged at consistently
higher temperatures than the other species (– 7.5 to – 8 8C).
Agathis atropurpurea, A microstachya and A. heterophylla
were the least cold tolerant, with average FT50 values in the
range of approx. – 5.5 to – 7.5 8C. Agathis robusta, A. bidwillii
and A. cunninghamii were damaged in the range –7 to – 9 8C,
and W. nobilis did not show significant damage until – 10.5 to
– 11 8C. In the high temperature experiment, FT50, mirrored by
slightly higher LT50 values of W. nobilis occurred at significantly
(P , 0.05) lower temperature (approx. 47.5 8C) than for
A. bidwillii and A. cunninghamii (48.5 – 52 8C) which was
lower than A. robusta, A. microstachya and A. heterophylla
(50.5– 53.5 8C). The initial and 100 % values generally mirrored
this pattern.
It can clearly be seen that in the upper temperature range,
FT50 was consistently lower than LT50, with the obverse
pattern in the lower temperature range (Fig. 2).
The Tspan, indicating the temperature tolerance range of each
species, was consistent between the two variables (Table 3).
All species had a temperature tolerance range between
58 and 61 8C.
TA B L E 3. The temperature tolerance span (Tspan) for Australian
Araucariaceae (from upper and lower LT50 estimates determined
by FvFm and visual rating, Fig. 2)
Tspan Fv/Fm
Tspan visual rating
58
59
61.5
58.5
57.5
58.5
58.5
58
59.5
60
59
59
59.5
59
Agathis atropurpurea
Agathis microstachys
Agathis robusta
Araucaria bidwillii
Araucaria cunninghamii
Araucaria heterophylla
Wollemia nobilis
Canopy vs. screen temperature
The effect of localized radiant heat is demonstrated in
Fig. 3. Meteorological screen temperatures recorded approx.
1 km away from the trees at Camden (BoM) on the observation
days were consistent with the temperatures recorded in the
shaded canopy of the trees. The exposed western side of the
trees had consistently higher temperatures. Temperature differentials between the eastern and western parts of the canopy of
5 –10 8C were recorded on the hotter days (Fig. 3). Using a
10 8C radiant heat factor, estimates of upper temperature
352
Offord — Temperature limits for relictual rain forest Araucariaceae
Screen
Eastern side of tree
Western side of tree
40
Temperature (ºC)
35
30
25
20
1
2
3
4
5
6
7
8
Day
9
10
11
12
13
F I G . 3. Maximum daily temperatures measured in late February 2009 within the canopy of Araucariaceae trees grown at Mount Annan Botanic Garden compared with the closest meteorological screen temperature (Campbelltown-Mount Annan, Australian Bureau of Meteorology, 2009).
limits for the species were determined using LT50 values
(Table 4). Maximum BoM screen temperatures ranged from
38.5 8C for W. nobilis to 43.5 8C for A. microstachya and
A. heterophylla.
TA B L E 4. Predicted upper meteorological screen temperature
limits based on LT50 (temperature at which leaves sustained 50
% damage; based on visual rating) (Fig. 2) +10 8C radiant heat
factor (Fig. 3)
Upper screen temperature limit (8C)
Ice nucleation temperature
All species showed a greater resistance to low temperature
exposure when the plants were winter-hardened (Table 5).
Ice nucleation occurred in leaves of A. heterophylla at only
– 2.5 8C in unhardened plants, but winter-hardened leaves
withstood similar temperatures to the other species, indicating
that some species are naturally more susceptible to ice nucleation when in the unhardened state. Ice nucleation did not occur
in winter-hardened A. microstachys until – 6.2 8C and in
W. nobilis until – 6.8 8C (Table 5).
DISCUSSION
Measuring thermal tolerance
There was generally good agreement between the two techniques used to determine leaf damage caused by low and
high temperatures. Fv/Fm is thought to overestimate the
lower temperature tolerance (Neuner and Buchner, 1999) and
underestimate the upper temperature tolerance (Bigras,
2000), the magnitude of which was similar in each of the
species examined here (Fig. 2) and by Cunningham and
Read (2006). Both Fv/Fm and visual rating can, therefore, be
taken as reliable measures of leaf damage due to temperature
in these species.
Fv/Fm values have been shown to correspond to whole plant
damage and mortality due to freezing (Percival and
Henderson, 2003). Several studies have identified chlorophyll
fluorescence (Fv/Fm) as the most useful from an array of
more conventional techniques used to study cold (MacRae
Agathis atropurpurea
Agathis microstachys
Agathis robusta
Araucaria bidwillii
Araucaria cunninghamii
Araucaria heterophylla
Wollemia nobilis
43
43.5
42.5
42
41
43.5
38.5
TA B L E 5. Exotherm
temperature
of
summerand
winter-hardened detached leaves of the seven Australian
Araucariaceae species
Species
Agathis atropurpurea
Agathis microstachys
Agathis robusta
Araucaria bidwillii
Araucaria cunninghamii
Araucaria heterophylla
Wollemia nobilis
Summer (8C)
Winter (8C)
–3.1ab
–4.6cd
–4.9d
–3.8ac
–3.5a
–2.5b
–4.6c
–6.6a
–6.2ac
–5.7bc
–5.5b
–5.5b
–5.7bc
–6.8a
Means within each column with the same letter are not significantly
different by l.s.d. (P . 0.05). Summer and winter means were significantly
different for each species.
et al., 1986; Perks et al., 2004) as well as heat tolerance
(Neuner and Pramsohler, 2006). The ability of this technique
to reflect irreversible tissue damage is because reversible
PSII damage may occur to a certain threshold beyond which
regulatory processes cannot cause a reversal and the
Offord — Temperature limits for relictual rain forest Araucariaceae
measurement is only detecting irreversible damage, which
happens rapidly past that critical point (Perks et al., 2004),
as estimated by FT50.
The degree of hardening and the sensitivity of the organ to
temperature would vary greatly in natural environments and so
these estimates, taken at the most acclimated point, reflect only
the possible thresholds for these species and not absolute
values. Further, these temperature tolerance values and rankings should be used as indicators of relative frost tolerance,
as frost tolerance varies greatly according to degree of cold
acclimation (‘hardening’) and provenance of the plant (Read
and Hill, 1989; Larmour et al., 2000). Frost severity in the
field depends on microtopography and exposure to the sky
(see King and Ball, 1998). While such factors may affect the
thermotolerance range of species, the comparison of wellacclimated plants from a common garden environment is
likely to be the best guide to the relative vulnerability of the
species to temperature extremes. This is borne out by the consistent temperature span of the species tested here which varied
by no more than 3.5 8C (Table 3) regardless of the estimates
for minimum or maximum temperatures. In their natural
environment, it is the ability of these species to acclimate
that will determine their response to climate change.
What are the temperature limits of Australian Araucariaceae?
This study confirms that Australian Araucariaceae are
mildly frost tolerant and may survive temperatures in the
range –5 to – 10 8C, with W. nobilis appearing to be the
most frost tolerant and the least heat tolerant. Agathis atropurpurea, A. microstachya and A. heterophylla were the least cold
tolerant and the most heat tolerant species. It might be
expected that A. bidwillii would be more cold tolerant than
A. cunninghamii, based on the lower temperatures experienced
in the wild (Table 1), but in this study the two species appear
to have similar low and high temperature responses and, along
with A. robusta, are the next most cold tolerant of the species
tested. These results are consistent with their current locations
and climatic regimes: W. nobilis, for example, occurs the furthest south and at an altitude of 900 m, while A. heterophylla
occurs on an island devoid of frost. The A. bidwillii provenance used was from a low altitude site, whereas the
A. cunninghamii was originally collected from a high altitude
location (Table 1). This does not explain why Sakai et al.
(1981) found A. bidwilli able to tolerate – 10 8C and
A. cunninghamii
– 5 8C. Araucaria bidwillii and
A. cunninghamii are the most widespread of the Australian
Araucariaceae, and it is likely that there are differences
between provenances that were not specifically tested in
either study. Further examination of the differences between
provenances would reveal the extent of temperature tolerance
in such widespread species. It has been suggested that
species with a wide geographic and altitudinal spread, such
as Nothofagus cunninghamii, have a wider thermal tolerance
than species with a narrower distribution (Howard and
Ashton, 1973). The consistency of the temperature tolerance
range for each of the species tested (57.7 – 61.5 8C, Table 3),
and for other Australian rain forest species studied by
Cunningham and Read (2006) which have similar temperature
tolerance ranges of about 60 8C, indicates that the wide
353
temperature tolerance observed in N. cunninghammii, for
example, is due to differences in temperature response
among provenances (Read and Busby, 1990).
According to the scheme of Larcher (2005), the Australian
Araucariaceae may be classified as ‘tropical – typical of
species from mountain forests’ (leaf threshold injury temperatures – 4 to – 12 8C) through to ‘temperate climate with mildwinter’, otherwise classified as Southern Hemisphere conifers
(– 10 to – 20 8C). Threshold injury temperatures (Fig. 2) for
W. nobilis place this species in the upper end of tropical and,
possibly, the lower end of the Southern Hemisphere conifer
category which experiences mild winters. This is consistent
with its southerly location and exposure to lower winter temperatures (Table 1).
While there were significant differences among the species
in response to high and low temperatures, all were within the
effective tolerance range of temperate and tropical species of
around 60 8C (Cunningham and Read, 2006), regardless of
which technique was employed (Fig. 2). The Fv/Fm and
visual rating together indicate that the leaves of winterhardened Australian Araucariaceae species are critically
damaged (as estimated by LT50) at temperatures below
– 5 8C and above – 11 8C (Fig. 2). This indicates that these
species are suitable for the zone described by Larcher
(2005) as having ‘episodic frosts with temperatures down
to – 10 8C’, which includes most of Australia, with the exception of the coastal tropics and the alpine areas. Rarely would
these species experience temperatures in wild populations as
low as these estimated LT50 values (Table 1), but the temperatures causing initial damage may be occasionally
reached (Fig. 2).
Winter cold resistance in evergreen Southern Hemisphere
species has been shown to be imparted by tolerance to extracellular ice formation (Neuner and Bannister, 1995). Many
temperate conifers avoid freezing-induced xylem cavitation
by having relatively small volume solute conduits compared
with deciduous species (Sperry and Sullivan, 1992; Feild
and Brodribb, 2001). Wollemi pine, for example, is an evergreen conifer that is considered to be temperate in origin
(Offord and Meagher, 2001) and has narrowly constricted
xylem structure at its branch base (Burrows et al., 2007),
and thus presumably has a high xylem pressure which would
decrease the chances of stem cavitation occurring due to freezing of xylem sap. Among the Araucariaceae, W. nobilis has the
most restricted xylem vessels (Burrows et al., 2007; Brodribb
and Feild, 2000), and its Huber value (xylem transverse sectional area per leaf area unit) is among the lowest recorded
for Gymnosperms (Burrows et al., 2007). This would
suggest that the Wollemi pine is the most adapted of these
species to avoidance of frost damage. Other functions of this
xylem restriction may include the facilitation of branch shedding (Burrows et al., 2007), or hydraulic control in response
to drought and minimization of cavitation (Brodribb and
Feild, 2000). An investigation of the xylem characteristics
across the Australian Araucariaceae, as suggested by
Pittermann and Sperry (2003), is greatly warranted. Such a
study may reveal much about the evolution of the tracheid
diameter and its relationship to cavitation avoidance, and, in
the context of this current study, to the water relations and
growth capacity of these species under climate change.
354
Offord — Temperature limits for relictual rain forest Araucariaceae
What does this mean for cultivation?
Minimum survival temperature (‘low temperature tolerance’, ‘cold tolerance’, ‘frost hardiness’, ‘freeze resistance’
or ‘frost resistance’) is often the main, if not the only, determinant of cultivation zones of many species (DeGaetano and
Shulman, 1990). Determination of climatic zones for cultivation is often based on climatic information of natural populations and rarely on physiological response, and many
species may be tolerant of temperatures outside their natural
range.
Ice nucleation temperature proved a useful guide for determining the relative freezing temperature of the leaves acclimated at high and low temperatures (Table 5). While it did
not detect major differences between the species, it is likely
that this is an accurate estimation of the true freezing temperature of the detached acclimated leaf (Bannister, 2007). The
marked difference experienced between winter-hardened and
summer-exposed leaves indicates that these Araucariaceae
species, along with many others studied (see for examples
Larcher, 2005), undergo acclimatization to lower temperatures
brought about by gradual exposure to sub-zero temperatures.
The relative inability of ice nucleation temperature to differentiate among different cold-hardened Araucariaceae species
may be explained by the ability of their photosynthetic apparatus to recover or protect the leaf from damage, even after the
apoplastic freezing point, as can be measured by Fv/Fm. It is,
therefore, the ability of the species to recover from freezing
events that determines their relative cold hardiness. Species
that are ice intolerant have ice nucleation temperatures
similar to their lethal damage values, while ice-tolerant
species can survive temperatures lower than their ice nucleation temperature (Bannister, 2007). Wollemi pine has an ice
nucleation temperature 3.5 – 4.2 8C lower than its LT50,
suggesting that leaf tissue of this species is ice tolerant to
some degree when winter hardened and is the most cold tolerant of the Australian Araucariaceae.
In terms of low temperature tolerance, visual rating places
these species in Plant Hardiness Zone 2 for Australia (the tablelands of south-east Queensland, New South Wales and Victoria)
(Dawson, 1991). For A. atropurpurea, A. microstachya,
A. heterophylla and possibly A. bidwillii, this equates to USA
plant hardiness Zone 9 (– 6.6 to – 3.9 8C) (US National
Arboretum, 1990); for A. robusta and A. cunninghamii Zone
8b ( –9.4 to – 6.6 8C); and, for W. nobilis Zone 8a ( – 9.4 to
– 12 8C). Care should be exercised when using temperature as
the determinant of plant ‘hardiness’, however, as soil moisture
and other factors also influence the suitability of a species for
a location (McKenney et al., 2007).
Threshold injury temperatures for Southern Hemisphere
conifers (from temperate climates with mild winters) indicate
that Australian Araucariaceae might withstand minimum
temperatures in the range – 5 to – 25 8C, depending on the
organ affected and the timing of the frost event (Sakai et al.,
1981; Larcher, 2005). The results from this present study indicate that all species tested were within this range when winter
hardened, but had a consistent pattern of response between
summer and winter. Where plants are gradually exposed to
lower and lower temperatures, many species become increasingly tolerant of low temperatures and may be induced to
harden beyond the normal range experienced in the wild.
Cultivated species are often grown at the limits of their tolerance. All the species tested showed greater cold temperature
tolerance during colder weather when compared with peak
summer, the difference being in the order of between 1 and
3.5 8C depending on the species.
While the specimen trees used in this study were from
reasonably protected positions, trees of A. robusta,
A. heterophylla and W. nobilis growing in exposed positions
in high light exhibit symptoms of photoinhibition – yellowing
characteristic of chlorophyll bleaching and leaf drop (Dungan
et al., 2003) – in several locations at The Australian Botanic
Garden, Mount Annan. While screen temperatures of –4 8C
are common at this location, it is likely that wind-chill and
localized temperatures, especially on exposed hillsides, may
be much lower than recorded screen temperatures. In the
case of A. robusta, and A. heterophylla in particular, the temperatures are likely to drop below the threshold for damage in
winter. In the case of W. nobilis, at least, canopy temperatures
were recorded that exceeded the critical temperatures for
damage, and this may account for the commonly reported
loss of this species in high light –high temperature situations
in Australia, reinforcing the advice that this species be
grown in protected positions (Offord and Meagher, 2006).
. . . And under climate change?
Ancestors of the extant conifer family Araucariaceae
evolved .200 million years ago and peaked in abundance in
the Jurassic (approx. 165 million years ago) (Stockey, 1982).
Extant species have higher optimal growth temperatures than
other temperate species and generally occur at lower elevations
than North American conifers which are often adapted to subalpine conditions (Hawkins and Sweet, 1989). In New
Zealand, there is evidence that Kauri survived both warming
and cooling periods, through at least 20 glacial events
(Mildenhall, 1980). Having survived many climatic regimes,
extant Araucariaceae appear to possess the ability to adapt to
changes in temperature over long periods of time. Short-term
changes, such as anthropogenic climate change, however, are
likely to affect significantly the ability of these species to
survive.
The results of this study suggests that, under current climate
change scenarios, high temperatures, rather than low temperatures, are likely to be a major determinant of future species distribution in natural populations. Evidence that low
temperatures are not currently limiting these species in the
wild is that most LTi values and all LT50 values (Fig. 2)
were lower than the lowest recorded temperature values
(Table 1). Although low temperatures are likely to be somewhat limiting in combination with high light, poor soil, low
rainfall and other factors that contribute to water stress (Sun
and Sweet, 1996), upward shifts in air temperature are likely
to damage leaves and other plant parts significantly (Allen
et al., 2010). For example, the highest recorded canopy temperature at Wollemi pine site 1 (see Offord and Meagher, 2001
for general climate description) over an 8 year period (1998–
2006) was 34.8 8C (unpublished data). Given a localized
radiant heat factor in the canopy of up to 10 8C (Fig. 3;
Offord — Temperature limits for relictual rain forest Araucariaceae
Larcher, 2000; Barker et al., 2005), little damage is likely to
result. If overall air temperatures in Australia were to be in
the order of 5 8C higher in 60 years time (CSIRO, 2010),
however, significant damage may result due to localized
canopy temperatures of approx. 49 8C, and the LT50 for this
species may therefore be reached. In cultivation, it is very
likely that this critical temperature is often reached or
exceeded in many situations, which may explain plant loss
in otherwise ideal situations. While the evidence shows that
Wollemi pine is the Araucariaceae species most vulnerable
to upward temperature shifts, other species may also be
affected to some degree.
All species have an optimal thermal range for photochemical activity. For example, measurement of Quercus ilex electron transport rates show that, for this species, the optimal
leaf temperature range is 15– 35 8C and temperatures on the
margins and outside this range result in leaf stress (Larcher,
2000). Warming per se may not compromise growth and survival for all species and may in fact enhance growth potential
for some species, particularly deciduous species (Way and
Oren, 2010). However, tropical rainforest species may be
more vulnerable than temperate rainforest species as they are
often operating with limited heat tolerance ranges and
may be less adaptable to upward shifts (Cunningham and
Read, 2003).
Another serious consequence of higher overall temperatures
might be a lack of, or insufficient, cold hardening. It is not yet
known what effect climate change will have on the frequency,
severity and distribution of frost events; however, it is likely to
drive extinctions or influence geographical distributions,
through primary and second order effects (Inouye, 2000).
Frost experienced by unhardened plants is likely to be catastrophic; if freezing occurs unseasonally, plants are more at
risk (Loik et al., 2004; Augspurger, 2009). It is not known
how long it takes Araucariaceae species to acquire frost hardiness; however, the acquisition of low temperature tolerance
through mild incremental exposure is well documented
(Odlum and Blake, 1996; Zhang et al., 2003). It is known
that, in some species, sugar concentration plays a role in
frost hardiness (Leborgne et al., 1995) while no relationship
is found in others (Zhang et al., 2003). Ice nucleation
temperature in this study was useful in demonstrating the
large difference between cold-hardened and unhardened
plants. Unhardened, ice nucleation temperatures of all
Australian Araucariaceae species are much higher than winterhardened tissues (Table 5). This indicates a level of cold
acclimation that has developed in response to exposure to
lower temperature, resulting in morphological and biochemical
changes, such as accumulation of carbohydrates and amino
acids (Alberdi and Corcuera, 1991). Interestingly, the greatest
difference between the two contrasting seasons was observed
for A. heterophylla (a difference of 3 8C). This might indicate
that this species has a greater capacity for thermal acclimation
than the other species, suggesting a temperate origin and
explaining its ability to acclimate to a variety of cultivated
situations, regardless of its relatively high low-temperature
tolerance threshold.
Phenological development is important to the severity of
frost damage (Miranda et al., 2005); damage to the leaves/
stem can be exacerbated by pruning and regrowth of leaves
355
prior to frosting events (Chappell et al., 2006). Climate variations, such as those projected under increasing greenhouse
gas models, may well shift the timing of cold events, such
that unhardened plants are exposed to low temperatures
outside normal seasons. This may lead to reversible or irreversible damage and will be a determinant of where a
species may be grown. The direction and extent of temperature
change are difficult to predict. It is certain that Australian
Araucariaceae species cannot be grown in very cold climates
without protection and, while sharp downwards shifts are not
anticipated, the species are more likely to be affected by
subtle shifts, i.e. early, late or severe and repeated frosts.
Frost de-hardening during spring may also render plants vulnerable to subsequent frosts, especially as warmer weather
may have hastened new leaf growth (Saxe et al., 2001).
Conservation implications
Given the already generally limited natural distributions of
Araucariaceae, these results suggest that climate change,
specifically temperature, rainfall and seasonality changes,
will increase the vulnerability of these species which are
already at the limits of their distribution and generally few
in number. The relatively naturally rare southern, more temperate Australian Araucariaceae, i.e. A. heteorphylla and
W. nobilis, are already more restricted in their distribution
than the more widely distributed more tropical species. Of
the Araucariaceae that occur in Australia, A. robusta,
A. bidwilli and A. cunninghamii are likely to be the most
adaptable, displaying diversity and a range of ecotypes
across their distributions (Whitmore and Page, 1980; Graham
et al., 1996; Peakall et al., 2003: Pye and Gadek, 2004),
which may extend to variability in temperature extreme tolerance as it does to the optimal temperature range for photosynthetic efficiency (Hill et al., 1988).
The role of ‘refugia’ in persistence of these species under
climate change is dependent on what the refugia will
provide. Wollemia nobilis is currently housed in microrefugia
(Ashcroft, 2010), in deep, protected gorges which may,
under climate change, warm more than the surrounding areas
due to their elevation, the effect of which may be mitigated
by cooling because of topographic shelter (Ashcroft, 2008).
Predicting the role of refugia may be problematic for these
species, and conservation actions, such as ex situ conservation
of Wollemi pine, for example (NSW Department of
Environment and Conservation, 2006), may therefore provide
refuge in the face of uncertainty (Rull, 2009). In the face of
climate change, moving a species to a cooler environment
but maintaining connection with essential or reliant biota
and edaphic requirements of the species is one option for
ensuring species survival (Westoby and Burgman, 2006).
More information is required to determine the effects of
temperature changes, in combination with other influential
growth parameters, particularly the effects of drought, on the
ability of these species to survive or adapt, and therefore to
predict accurately and confidently future distributions
(Beaumont et al., 2005) and to plan appropriate management
strategies. Westoby and Burgman (2006) discuss future management options for species threatened by climate change,
such as the ‘do nothing approach’, translocation to a more
356
Offord — Temperature limits for relictual rain forest Araucariaceae
suitable location and, preferably, minimizing warming. The
thermotolerance ranges of species, such as those determined
in this study, are useful parameters for this process even
though these data represent just snapshots.
AC KN OW LED GEMEN T S
Patricia Meagher and NSW Parks and Wildlife staff are
thanked for site climate data collections. John Silk provided
technical support for collection of material. Karen
Sommerville, Kim Hamilton and two anonymous reviewers
contributed helpful comments on the manuscript.
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