Trees (2011) 25:925–934
DOI 10.1007/s00468-011-0567-5
ORIGINAL PAPER
Continental-scale climatic drivers of growth ring variability
in an Australian conifer
David M. J. S. Bowman • Lynda D. Prior •
David Y. P. Tng • Quan Hua • Timothy J. Brodribb
Received: 14 December 2010 / Revised: 3 March 2011 / Accepted: 11 April 2011 / Published online: 24 April 2011
Ó Springer-Verlag 2011
Abstract Callitris is Australia’s most successful and
drought tolerant conifer genus. Callitris species are distributed across a huge geographical range from rainforest
to arid zones, and hence they provide a rare opportunity to
view plant growth trends across the continent. Here, we
make a continental-scale examination of how climate
influences basal diameter growth in Callitris. We sampled
a total of five species but focused effort (23 of 28 samples)
on the most widespread species, C. columellaris. Cores
from a total of 23 trees were sampled from 15 sites that
spanned a gradient in mean annual rainfall from 225 to
2117 mm and mean annual temperature from 11.5 to
28.2°C. Ring production is not annual across much of the
distribution of the genus, so 14C-AMS dating was used to
establish the frequency of ring production for each core.
Ring width, tracheid lumen diameter and number of tracheids per ring were also measured on each core. Ring
production was close to annual at mesic sites with reliable
alternation of rainfall or temperature regimes but was more
erratic elsewhere. For C. columellaris, ring width significantly increased with mean annual rainfall (r2 = 0.49) as a
result of wider and more tracheids per ring. For this species
tracheid lumen diameter was correlated with annual rainfall
(r2 = 0.61), with a threefold increase from the driest to the
Communicated by A. Gessler.
D. M. J. S. Bowman (&) L. D. Prior D. Y. P. Tng T. J. Brodribb
School of Plant Science, University of Tasmania,
Private Bag 55, Hobart, TAS 7001, Australia
e-mail: [email protected]
Q. Hua
Australian Nuclear Science and Technology Organisation,
Locked Bag 2001, Kirrawee DC, NSW 2232, Australia
wettest sites, lending support to the hypothesis that conifers
growing at drier sites will have narrow lumen diameters to
maximise mechanical strength of the xylem.
Keywords Callitris columellaris Tree growth Rainfall Tracheids Lumen diameter
Introduction
Dendrochronologists use growth responses of trees to
investigate temporal variability in climate by using crossdating, a technique which relies on a growth response that
is synchronised and similar amongst a population of trees
at a particular site (Fritts 2001). They have traditionally
focussed on trees growing on sensitive sites, often at the
limit of their climate ranges. However, there are many sites
with low climatic seasonality, where individual tree
responses are variable or unresponsive to climate variation
(Fritts 2001; La Marche et al. 1979). These sites have
generally been avoided by dendrochronologists, yet they
constitute ecosystems that are amongst the most globally
important and vulnerable to climate change. Although trees
in these environments may not cross-date, they can still
yield important insights into the influence of climate on
tree growth per se (Enquist and Leffler 2001; Fichtler et al.
2003; Brienen and Zuidema 2005; Dulamsuren et al. 2010).
In most Southern Hemisphere lowland environments,
including much of Australia, winters are mild and rainfall
occurs unpredictably in any season and consequently the
tree flora is dominated by evergreens (Bowman and Prior
2005). In these environments, evergreen trees tend to grow
opportunistically in response to sporadic rainfall events
rather than producing annual growth rings (Pearson et al.
2011), thus limiting the classical dendrochronological
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926
potential of the Australian tree flora (La Marche et al.
1979). However, radiocarbon dating can provide independent validation of dates obtained from dendrochronology
(Hua et al. 1999) because above-ground nuclear detonations between 1945 and 1980 injected a large amount of
14
C into the upper atmosphere, with atmospheric 14C
concentration in organic materials peaking in the mid
1960s. This well-documented pattern of atmospheric 14C
concentration allows dating of individual tree rings from
the 1960s with a resolution of one to a few years (Hua and
Barbetti 2004; Hua 2009; Searson and Pearson 2001;
Vieira et al. 2005; Pearson et al. 2011). 14C dating has also
been used to validate the annual nature of ring growth of
several tropical tree species (Fichtler et al. 2003; Worbes
et al. 2003; Biondi et al. 2007). The technique therefore
enables analysis of growth events over the last four to five
decades, and thereby calculation of average annual growth
rates.
The conifer flora is generally less prominent in Australia
than in other continents. An important exception is the
genus Callitris (Cupressaceae), which is broadly distributed across a range of Australian environments in tropical,
cool temperate, Mediterranean and arid climatic zones
(Bowman and Harris 1995). Associated with the very wide
ecological range of Callitris in Australia is the fact that this
genus is probably the most drought resistant tree genus on
Earth (Brodribb et al. 2010). Drought resilience gives
Callitris species the ability to survive droughts and attain
ages typically [200 years. In addition, these trees are of
considerable dendrochronological interest given their distinct growth rings, relative longevity and termite resistance,
resulting in old trees possessing long sections of sound
wood (Bowman and Panton 1993). In the Australian seasonal tropics, annual ring production has been demonstrated for both C. macleayana (Ash 1983) and
C. intratropica (syn. C. columellaris; Baker et al. 2008). In
both cases, ring width was positively correlated with the
length of the wet season, indicating that growth is primarily
limited by water availability (Baker et al. 2008). Annual
ring production at these mesic tropical sites is unsurprising
given that rainfall is both reliable and extremely seasonal.
However, in drier tropical regions where wet season rainfall is less reliable, tree growth is likely to be more erratic,
as has been observed in arid and semi-arid areas of temperate Australia. For example, in one of the first studies of
tree rings in arid Australia, Lange (1965) found that ring
production in C. glaucophylla (syn. C. columellaris) was
inconsistent among trees; during some periods, it averaged
[1 ring per year, and \1 ring per year at other times. By
contrast, in the wetter, colder environment of Kosciuszko
National Park, C. glaucophylla (syn. C. columellaris) trees
generally produced distinct annual growth rings in response
to low winter temperatures, but there were also irregular
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Trees (2011) 25:925–934
intra-annual rings, probably resulting from low soil moisture at times during the warmer seasons (Banks and
Pulsford 2001). Most recently, Pearson et al. (2011) confirmed that ring formation was close to annual in the seasonal tropics but irregular in arid environments.
The connection between tree growth, tree ring formation
and climate is rarely the focus of dendrochronological
studies, although these linkages are of interest to tree
physiologists. For example, climate is known to influence
the dimensions of tracheids in conifer wood, particularly
lumen diameter. Protection of conifers from droughtinduced embolism is correlated strongly with lumen diameter due to the dominant influence of thickness-to-span
ratio, the double-wall thickness per lumen diameter (Sperry
et al. 2006; Pittermann et al. 2006). Sperry et al. (2006)
argued that conifers growing in arid environments require
stronger tracheids with a greater thickness-to-span ratio,
and predicted they should have narrower lumen diameters
because cell walls should be as thick as possible to maximise conducting efficiency for a given mechanical strength.
Here, we estimated growth rates and frequency of growth
events of Callitris trees growing in contrasting climates by
combining ring width measurements and accelerator mass
spectrometry (AMS) 14C dating. We then related these
growth rates to mean annual rainfall, rainfall seasonality,
intra-annual rainfall variability and mean annual temperature. We also examined the effect of climate on the tracheid
lumen diameter of trees growing in these contrasting environments, to determine whether tracheid lumen diameters
are smaller in regions subject to greater water stress, in line
with the predictions of Sperry et al. (2006).
Methods
Study sites and species
For this work, we selected tree cores sampled during a
series of studies of Callitris across Australia, building on
the survey of Pearson et al. (2011) and Prior et al. (2011).
Study sites were chosen to represent a wide range of
climates across Australia, and included seven tropical,
seven arid and four temperate sites (Fig. 1; Table 1). We
were especially interested in tropical sites at which either
the dry season or the wet season is shorter and less extreme
than near Darwin, Litchfield and Arnhem Land, where
annual ring formation has been demonstrated (Baker et al.
2008; Pearson et al. 2011). We therefore sampled in the
Kimberley, NT Gulf and wet-dry tropics of Queensland (all
have less reliable wet season rainfall than the Darwin
region) and in the wet tropics of Queensland (a less pronounced dry season). In addition, the Darwin region was
also sampled to confirm annual ring formation in trees
Trees (2011) 25:925–934
Fig. 1 Location, climate and Callitris species found at sampling
sites. Mean annual rainfall for the continent is also shown. The small
graphs indicate mean monthly maximum and minimum temperatures
there (Fig. 1). We also aimed to investigate frequency of
growth events in temperate Australia including desert
environments in central Australia to the humid sub-tropics
of New South Wales and temperate maritime climates in
Victoria and Tasmania. However, we were unable to use
the most arid sites we had sampled because rings of cores
taken from these sites were too narrow to provide sufficient
material for AMS dating. In total we measured 23 cores
from Callitris columellaris (sensu Farjon 2005), the most
widespread species in the genus. To provide a context for
the sampled Callitris columellaris we also included samples from a range of other Callitris species (Fig. 1;
Table 1).
Climate data
Monthly temperature and rainfall data were obtained from
the nearest weather station with a record [30 years
(Bureau of Meteorology 2010a). The rainfall seasonality
index (SI) of Walsh and Lawler (1981) was calculated from
these meteorological data:
927
(solid and open symbols, respectively) and rainfall (grey bars), with
month on the x axis (month 1 is January, month 12 is December). Site
and sample details are listed in Table 1
12 R 1X
SI ¼ xn 12
R
n¼1
where R is mean annual rainfall and xn is the mean rainfall
of month n.
To obtain coefficients of variation for inter-annual
rainfall that was comparable for all locations, we used
annual rainfall data collected over the same period generated by the Bureau of Meteorology’s Interactive Australian
Rainfall and Surface Temperature portal (Bureau of
Meteorology 2010b). This database provides spatially
averaged monthly rainfall values from 1,900 onward based
on all data available for each region. We used 1° cells, the
maximum available spatial resolution. The climate of each
sample site was classified according to the Köppen–Geiger
system (Kottek et al. 2006).
Core sampling
At each site, trees were selected to minimise ring width
variation related to local changes in topographic, edaphic
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Trees (2011) 25:925–934
Table 1 Sampling location and species of each core used in AMS dating, ANSTO code (OZ No.), mean annual rainfall (MAR), coefficient of
variation (CV) for annual rainfall, rainfall seasonality index (SI), mean annual temperature (MAT) and climate classification based on the
Köppen–Geiger scheme
Location
Latitude Longitude Species
°S
°E
OZ no. for
Sample
1
Elevation MAR CV SI
(m)
(mm) (%)
MAT Climate
(°C) (Köppen-Geiger)
2
North Queensland 1
16.85
145.64
C. columellaris M432 M433
390
2117 26.8 0.76 24.9
Tropical monsoonal (Am)
Litchfield 1, NT
13.47
130.68
C. columellaris G418 H087
16
1533 18.0 0.99 27.3
Tropical wet–dry (Aw)
Litchfield 2, NT
12.97
130.65
C. columellaris G417 NA
46
1533 18.0 0.99 27.3
Tropical wet–dry (Aw)
North Queensland 5
17.27
145.42
C. macleayana M210 M211 1030
1379 26.0 0.73 20.5
Tropical wet–dry (Aw)
Arnhem Land, NT
12.36
134.19
C. columellaris K481 K482
9
1307 20.8 1.02 28.2
Tropical wet–dry (Aw)
NT Gulf
16.50
137.55
C. columellaris M382 M383
35
923 32.7 1.04 26.3
Tropical wet–dry (Aw)
Kimberley, WA
15.10
128.68
C. columellaris M384 M385
80
820 26.4 0.99 28.0
Tropical wet–dry (Aw)
North Queensland 2
17.56
145.15
C. columellaris M434
770
812 27.3 0.87 20.5
Tropical wet–dry (Aw)
North Queensland 3
18.81
144.86
C. columellaris K977 K978
752
763 27.3 0.85 23.6
Tropical wet–dry (Aw)
Moreton Island, Qld
Pilliga, NSW
27.19
31.26
153.37
148.93
C. columellaris NA
NA
C. columellaris M386 M387
60
400
1504 24.9 0.26 20.6
594 27.5 0.15 15.6
Humid subtropical (Cfa)
Humid subtropical (Cfa)
Pilliga, NSW
31.26
148.93
C. columellaris M388 M389
400
594 27.5 0.15 15.6
Humid subtropical (Cfa)
Pilliga, NSW
31.26
148.93
C. columellaris M390 M391
400
594 27.5 0.15 15.6
Humid subtropical (Cfa)
South-west WA
32.12
115.76
C. preissii
K491 K492
4
751 21.1 0.74 18.8
Mediterranean (Csa)
Maria Island, Tas
42.68
148.08
C. rhomboidea K487 K488
9
711 22.7 0.08 12.7
Maritime temperate (Cfb)
Maria Island, Tas
42.68
148.08
C. rhomboidea K489 K490
9
711 22.7 0.08 12.7
Maritime temperate (Cfb)
M435
Snowy River, Vic
37.08
148.42
C. columellaris K483 K484
203
685 18.3 0.15 11.5
Maritime temperate (Cfb)
North Queensland 4
18.99
146.05
C. endlicheri
K979 K980
780
655 34.1 0.86 23.6
Semi-arid hot (BSh)
Northern Victoria
36.00
144.21
C. columellaris K485 K486
110
393 27.9 0.17 15.9
Semi-arid warm (BSk)
Pilbara, WA
23.04
118.85
C. columellaris M374 M375
800
318 50.9 0.6
24.4
Arid hot (BWh)
Central Australia 2, NT 23.45
134.70
C. columellaris G416 H088
659
289 53.1 0.5
21.0
Arid hot (BWh)
Central Australia 2, NT 23.45
134.70
C. columellaris K478 NA
659
289 53.1 0.5
21.0
Arid hot (BWh)
Central Australia 3, NT 23.75
133.87
C. columellaris K479 NA
613
281 53.6 0.44 21.0
Arid hot (BWh)
Central Australia 3, NT 23.75
133.87
C. columellaris G851 H086
613
281 53.6 0.44 21.0
Arid hot (BWh)
Central Australia 1, NT 23.67
Central Australia 1, NT 23.67
132.65
132.65
C. columellaris G850 H089
C. columellaris K480 NA
644
644
273 53.1 0.5
273 53.1 0.5
21.0
21.0
Arid hot (BWh)
Arid hot (BWh)
Western NSW
30.98
142.29
C. columellaris M376 M377
170
225 48.8 0.21 19.8
Arid hot (BWh)
Western NSW
30.98
142.29
C. columellaris M378 M379
170
225 48.8 0.21 19.8
Arid hot (BWh)
Western NSW
30.98
142.29
C. columellaris M380 M381
170
225 48.8 0.21 19.8
Arid hot (BWh)
The meteorological data were obtained from nearby weather stations. Sites are sorted in order of decreasing rainfall within climate classes
NA not applicable
and other factors. All cored trees were mature canopy trees
more than about 50-years old. Multi-stemmed or unhealthy
trees were avoided. Ring widths of Callitris are affected
relatively little by tree size or by moderate inter-tree
competition, although they are markedly reduced by
intense competition (Horne 1990; L. D. Prior, unpublished
data). At each site, two cores were taken from each of 10 to
15 trees at *0.4–1.3 m above ground level using a 5 mm
diameter increment borer. Zones of obvious ring wedging,
reaction wood, or injury were avoided. Cores were extruded into plastic straws and sealed in the field. Standard
methods of core preparation were used (Stokes and Smiley
1968). All cores have been lodged at the Tasmanian
123
Dendrochronological
Tasmania.
Facility
at
the
University
of
AMS dating
Between one and three cores from each site were selected
for AMS radiocarbon dating, based on soundness and rings
that were wide enough to provide adequate material for
analysis. In most cases, two single tree-ring samples predicted by ring counts to have been produced between 1960
and 1974 were taken from each core for radiocarbon
analysis. A total of 52 samples of individual rings from 28
tree cores were extracted to alpha-cellulose for AMS
Trees (2011) 25:925–934
929
Table 2 Correlation coefficients between mean annual rainfall
(MAR), coefficient of variation (CV-rain) for annual rainfall, rainfall
seasonality index (SI-rain), mean annual temperature (MAT) and ring
MAR
MAR
CV-rain
SI-rain
CV-rain
width, rings per year, annual diameter increment, lumen diameter and
tracheids per ring, using data for all species
MAT
Ring width
Rings per year
Annual diameter
increment
1
20.70
0.41
0.49
20.50
0.05
20.70
1
0.08
20.60
0.31
-0.31
-0.20
0.89
0.58
20.52
0.12
-0.00
0.56
MAT
0.41
0.08
1
0.33
-0.32
Ring width
0.49
20.60
0.33
1
-0.29
0.64
20.50
0.31
-0.32
-0.29
1
0.38
Rings per year
Annual diameter increment
0.05
-0.31
-0.00
0.64
0.38
Lumen diameter
0.70
20.57
0.51
0.76
-0.37
0.41
Tracheids per ring
0.33
20.59
0.09
0.79
-0.19
0.64
1
Significant values (P \ 0.05) are shown in bold
analysis using the STAR facility at ANSTO (Fink et al.
2004; Hua et al. 2004). We could not use cores from the
wettest sub-tropical site (Moreton Island) because we were
unable to discern growth rings in these cores. Age calibration was performed using the CALIBomb programme
(Reimer and Reimer 2004; Reimer et al. 2004) and atmospheric bomb 14C data for the Southern Hemisphere (Hua
and Barbetti 2004).
Tree growth and ring counts
The total radial length of wood produced since the most
recent ring used for AMS dating was measured, and the
corresponding number of rings counted. For this work, no
attempt was made to class rings as annual or intra-annual
(‘false’), because we were interested in the frequency of
growth events in the contrasting environments, although
many of these samples have been cross-dated in a previous
study (Pearson et al. 2011). The average number of rings
formed per year and mean annual diameter growth were
then calculated.
Ring width, tracheid lumen diameter and tracheids
per ring
The same cores used for radiocarbon dating were sampled
for ring widths and tracheid lumen diameters and number
of tracheids per ring. The width of the most recent 100
growth rings in each core was measured by scanning the
cores at high resolution (1200 dpi) and processing the scans
with WinDendro (Regent Instruments Inc., Quebec City,
Canada), a tree ring image analysis programme. A total of
100 rings was assigned to each core and an output of the
ring widths of each core was generated. If the core had
fewer than 100 growth rings, all were measured. To obtain
estimates of lumen diameter and number of tracheids per
growth ring, a sequence of digital microphotographs (459
magnification) was taken of the sapwood region of each
core and processed in ImageJ (National Institute of Mental
Health, Maryland, USA), a Java-based imagine processing
programme. Starting from the bark, a transect was placed
longitudinally across the entire sapwood sequence,
including both latewood and earlywood cells. The number
of tracheids along the transect within each ring was
counted for every fifth growth ring, working inwards from
the bark. The lumen diameters of the first 300 tracheids
closest to the bark were measured to the nearest lm using
the line function in ImageJ. Damaged cells near cracks in
the core along the transect were avoided. Prior to measuring the tracheids, dimensional calibrations were made
by photographing a 1 mm graticule slide, using ImageJ to
draw a line across the 1 mm scale and calibrating the line
distance to denote 1000 lm.
Data analysis
Analysis of variance was used to test differences in
C. columellaris growth attributes among the major climate
zones (tropical, arid and temperate). Linear regressions
were used to determine relationships with mean annual
rainfall and mean annual temperature. Mean annual rainfall
and ring widths were log-transformed to normalise the
data.
Results
The climates sampled in our study were broadly classified
as tropical, arid or temperate (Table 1). The tropical sites
had the highest mean annual rainfall (up to 2117 mm) and
mean annual temperature (up to 28.0°C), the highest rainfall seasonality and among the lowest coefficients of
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Trees (2011) 25:925–934
b Fig. 2 Mean ring width, rings per year, diameter increment per year,
3
Ring width (mm)
2
median tracheids per ring and median tracheid lumen diameter versus
mean annual rainfall for all sampled cores. Solid symbols and
regression lines and correlation coefficients apply to C. columellaris,
and other species are represented by open symbols. All correlations
except that between diameter increment and rainfall were significant.
Note the log scale for mean annual rainfall and ring width
2
r = 0.49
1
0.8
0.6
0.5
0.4
variation in annual rainfall (Table 1). The arid sites had the
lowest mean rainfall (as little as 225 mm) with the highest
coefficient of variation in annual rainfall, and intermediate
rainfall seasonality and temperatures. The temperate sites
had the lowest mean annual temperatures (as low as
11.5°C), the lowest rainfall seasonality, amongst the lowest
variability in annual rainfall and intermediate mean annual
rainfall. Thus the climate variables were inter-correlated,
for example, the correlation coefficient between mean
annual rainfall and rainfall coefficient of variation was
-0.70 (Table 2).
Considering all samples together, we found that growth
events, and thus ring formation, generally occurred more
frequently than once per year, as shown by the divergence
between the putative age estimated from ring counting and
the age obtained from AMS analysis (Fig. 2). Ring formation was close to annual at the wetter sites (mean annual
rainfall [ *1000 mm) where rainfall is strongly seasonal,
but highly variable at lower rainfall sites with less predictable rainfall (Fig. 2, Table 2). Ring formation was also
close to annual at the temperate sites with a Mediterranean
or a maritime climate, but not at the humid, sub-tropical
sites (Fig. 3). The lack of distinct growth rings at Moreton
Island (the wettest sub-tropical site, with mild temperatures
year-round; Table 1; Fig. 1) suggests that growth is continuous at this site. There were no obvious differences in
0.3
Rings per year
2.0
1.8
r2 = 0.23
1.6
1.4
1.2
1.0
0.6
7
6
5
4
3
2
1
80
70
Tracheids per ring
r2 = 0.06
60
r2 = 0.35
50
40
2.2
30
2.0
20
1.8
Rings per year
-1
Diameter increment (mm y )
0.8
Tracheid lumen diameter (mm)
10
0
0.045
0.040
1000
r2 = 0.61
Tropical
Tropical, other
Arid
Arid, other
Sub-tropical
Mediterranean, other
Maritime
Maritime, other
1.6
1.4
1.2
1.0
0.8
0.035
0.6
10
0.030
15
20
25
30
Mean annual temperature (°C)
0.025
0.020
0.015
200
400
600
800 1000
Mean annual rainfall (mm)
123
2000
Fig. 3 The relationship between the mean number of rings produced
each year over the last 4 to 5 decades and mean annual temperature.
Solid symbols apply to C. columellaris, and open symbols to other
species. Within the temperate zone, ring production was close to
annual at the Mediterranean and maritime sites but not at the subtropical one
Trees (2011) 25:925–934
931
Arid
Temperate
Tropical
20
10
Ring width (mm)
5
2
1
0.5
0.2
0.1
0.05
300
200
150
100
50
0
0.06
0.04
Nth Queensland 1
Litchfield 1
Litchfield 2
Arnhem Land
NT Gulf
*Nth Queensland 5
Kimberley
Nth Queensland 2
Nth Queensland 3
Snowy R
*Maria Is b
*SW Western Australia
Pilliga c
*Maria Is a
Pilliga b
Pilliga a
*North Queensland 4
Pilbara
Northern Victoria
Central Australia 2a
Central Australia 2b
Central Australia 3b
Central Australia 1b
Central Australia 3a
Western NSW c
Central Australia 1a
0.00
Western NSW b
0.02
Western NSW a
Tracheid lumen diameter (mm)
Tracheids per ring
250
Fig. 4 Ring widths, number of tracheids per ring, and tracheid lumen
diameters of cores from the sampling locations shown in Table 1,
arranged within climate zones in order of increasing mean annual
rainfall. Sites marked with a star indicate species other than
C. columellaris. The boundary of the box closest to zero indicates
the 25th percentile, the line within the box marks the median, and the
boundary of the box farthest from zero indicates the 75th percentile.
Whiskers above and below the box indicate the 90th and 10th
percentiles, and the small circles represent the outliers. The numbers
1, 2, and 3, and the letters a, b, and c at the end of site names indicate
multiple sites within a region, and replicate cores within a site,
respectively. Note the log scale for ring width
growth attributes relative to rainfall and temperature
between C. columellaris and the other species (Fig. 4), but
to avoid possible complications due to species effects, our
data analyses focussed on C. columellaris.
Amongst the three climate zones, annual diameter
increment, number of rings produced each year, ring width,
number of tracheids per ring and tracheid lumen diameter
of C. columellaris all varied significantly (Table 3). For
example, annual diameter increment averaged 5.0 mm
year-1 at temperate sites compared with 3.5 and 2.4 mm
year-1 at tropical and arid sites, respectively. On average,
1.6 rings were produced each year at the temperate sites,
1.4 at the arid ones and 1.0 at the tropical sites, while rings
were widest at the tropical sites and narrowest at the arid
ones (Table 3). The wide rings at the tropical sites were
due to both large tracheid lumens compared with temperate
and arid sites, and to more tracheids per ring than the arid
sites (Fig. 2).
Ring width, tracheids per ring and tracheid lumen diameter of C. columellaris were all positively correlated with
mean annual rainfall (Fig. 2), but were not correlated with
mean annual temperature. The number of rings produced per
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Table 3 Diameter growth, number of rings produced each year, median ring width (all 100 measured rings/core), mean ring width (to the most
recent ring used for AMS dating), tracheids per ring and tracheid lumen diameter for C. columellaris only, averaged for each climate zone, with
standard errors
Climate zone
Diameter growth
(mm/year)
Rings per
year
Ring width (mm)
Median
(100 rings/core)
Mean
(to AMS sample)
Tracheids
per ring
Tracheid lumen
diameter (mm)
Tropical
3.50 ± 0.64
1.02 ± 0.06
1.66 ± 0.27
1.67 ± 0.26
43 ± 6
0.034 ± 0.002
Arid
2.37 ± 0.29
1.38 ± 0.12
0.55 ± 0.09
0.84 ± 0.09
23 ± 3
0.022 ± 0.001
Temperate
5.03 ± 0.70
1.59 ± 0.18
P
0.014
0.017
0.96 ± 0.09
\0.001
1.59 ± 0.11
44 ± 3
0.004
0.003
0.026 ± 0.002
\0.001
The diameter growth and the mean ring width to the AMS sample are based on the same section of each core. P values indicate the significance
of differences among climate zones
30
Mean annual temperature (°C)
year was negatively correlated with both mean annual
rainfall (Fig. 2) and mean annual temperature (Fig. 3),
reflecting the annual ring production at tropical sites compared with more frequent production at arid and temperate
ones. There was no overall correlation between annual
diameter increment of C. columellaris and either mean
annual rainfall (Fig. 2) or mean annual temperature, but if
tropical sites are excluded, there was a significant positive
relationship with mean annual rainfall (r2 = 0.50) and a
negative one with mean annual temperature (r2 = 0.39).
7
3
4
5
25
128
16
22
24
21
2
28
27
20
45
222
3
157
78
15
1
157
143
Discussion
89
35
10
0
500
1000
4
1500
2000
2500
Mean annual rainfall (mm)
Growth rings in Callitris were typically close to annual in
the wetter parts (mean annual rainfall [1000–1200 mm) of
the seasonal tropics and at the sites with a temperate
maritime or a Mediterranean climate, but appeared erratic
over the remainder of its range, especially in arid and semiarid climates. The determinant of growth appears to be
seasonal moisture supply in all cases except that of the
temperate maritime climate, where we suspect winter
temperatures are low enough to halt growth despite sufficient year round moisture. The Australian environments in
which tree growth was close to annual are similar to those
elsewhere with annual growth patterns, namely the northern hemisphere mid latitude zone, where dendrochronology
was developed, and the seasonal tropics (reviewed by
Rozendaal and Zuidema 2011) (Fig. 5). Our results from
cores sampled from the semi-arid tropics suggest that
rainfall is not sufficiently reliable to consistently generate
annual growth of Callitris stems, unlike the pattern in the
mesic seasonal tropics found using traditional dendrochronological analyses (Baker et al. 2008, Pearson et al.
2011). These findings are consistent with studies in Ethiopia showing annual growth rings of Juniperus procera are
formed at mesic sites with a unimodal rainfall regime (Wils
et al. 2011), but not where there is year-to-year variability
in the number of wet and dry seasons (Wils et al. 2009).
123
Fig. 5 Occurrence of annual ring formation in Callitris relative to
four types of climate delineated by dashed lines (where 1 arid,
2 seasonally dry, 3 wet tropical and subtropical, 4 cool temperate).
Annual ring formation (closed circles) is defined here as 0.9 to 1.1
rings per year. Open circles denote non-annual ring growth and the
star represents the site with continuous growth and no clear rings. The
small numbers next to the symbol refer to the mean rainfall (mm) of
the driest 3-month period at the site, to indicate the intensity of the dry
season. Callitris growth rings are most likely to be annual where
temperature does not limit growth and reliable wet and dry seasons
alternate annually (Type 2, corresponding to Köppen Aw and Csa)
and in areas with adequate water year-round but winter-limited
growth (Type 4, corresponding to Köppen Cfb). By contrast, growth
is unlikely to be annual (Type 1, corresponding to Köppen B), where
rainfall is not annually reliable, and growth is water-limited and
occurs in response to rainfall events. Conversely, there is no
pronounced dry season to annually restrict growth, and rings are
not annual and may be very indistinct in Type 3 (corresponding to
Köppen Am and Cfa)
Overall, the relationship between annual diameter
increment and mean annual rainfall was surprisingly weak,
and apparent only at drier sites (i.e., excluding the tropical
sites, where rainfall exceeds *750 mm). We acknowledge
that the sample size was necessarily limited by the expense
of AMS dating, and that core selection was biased towards
those with the widest rings, to provide enough material for
Trees (2011) 25:925–934
AMS dating. The sampling therefore provides an upper
bound of tree growth in lower rainfall areas. The remarkable drought tolerance of Callitris (Brodribb et al. 2010)
suggests that the trees may not grow for long periods if soil
moisture is limiting. Such drought tolerance explains why
more rings were produced per year on average at drier sites
than at more mesic ones: in arid sites the evergreen trees
opportunistically grow for a short period in response to
individual rainfall events. Such growth responses that
produce numerous ‘false’ rings clearly frustrate classical
dendrochronology. Further, it is also likely that the influence of other factors such as seasonal pattern and variability of rainfall, temperature and evaporative demand,
soil type and landscape position may interact with moisture
supply, confounding neat growth responses relationships
with annual rainfall.
Wetter sites produce wider rings because both tracheid
lumen diameter and the number of tracheids per ring are
higher than at dry sites. Median lumen diameter of tracheids increased almost three-fold from the driest to the
more mesic sites. Our results, obtained from a single species growing over a large climatic gradient, therefore
provide strong support for the hypothesis of Sperry et al.
(2006) that conifers in arid environments require strong
tracheids with small lumen diameters. This is because drier
environments are associated with more negative sap pressures, and tracheids require greater thickness to span ratios
to confer mechanical strength and resist implosion (Sperry
et al. 2006). Previous studies have yielded inconsistent
results: for example, drought stress reduced lumen area but
did not affect cell wall thickness of tracheids of Abies
balsamea seedlings (Rossi et al. 2009), but lumen diameters of Pinus sylvestris in drier regions of Spain were larger
than in more mesic areas (Martı́n et al. (2010). Our results
suggest that narrow tracheid lumens are a key adaptation of
Callitris trees to dry environments.
Acknowledgments We thank Scott Nichols, Phillip Moser, Diane
Prior, Lachie McCaw, Kim Whitford, Richard Fairman, Sharyn
Yelverton, Herman Mouthaan, Stephen Harris, Kim Webeck, Kathryn
Allen and Stuart, Kate, Lily and Ted Pearson for field assistance. Rob
Argent, Melbourne Water, collected the Snowy River sample. Scott
Nichols and Kathryn Allen prepared the cores, and Zoe Lee helped in
sample processing for AMS 14C analysis. Gregor Sanders prepared
the map. This project received funding from CERF grant B0016193.
Radiocarbon analysis was funded with grants from the Australian
Institute of Nuclear Science and Engineering (Grants 00/122, 03/090P
and 07/014). We thank the Northern Territory Parks and Wildlife
Service, NSW Department of Environment and Climate Change,
Queensland Department of Environment and Resource Management,
WA Department of Environment and Conservation, Victorian
Department of Sustainability and Environment, Parks and Wildlife
Service Tasmania, the Consolidated Pastoral Company, Mr Garth
Dunford, the Siemer family and the Australian Wildlife Conservancy
for help with site selection and permission to sample on their land.
933
References
Ash J (1983) Tree rings in tropical Callitris macleayana F. Muell
Aust J Bot 31:277–281
Baker PJ, Palmer JG, D’Arrigo R (2008) The dendrochronology of
Callitris intratropica in northern Australia: annual ring structure,
chronology development and climate correlations. Aust J Bot
56:311–320
Banks J, Pulsford I (2001) Dendrochronology of Australian cypress
pines. In: Dargavel J, Hart D, Libbis B (eds) Perfumed pineries.
Environmental history of Australia’s Callitris forests. Centre for
Resource and Environmental Studies, Australian National University, Canberra, pp 30–38
Biondi F, Strachan SDJ, Mensing S, Piovesan G (2007) Radiocarbon
analysis confirms the annual nature of sagebrush growth rings.
Radiocarbon 49:1231–1240
Bowman DMJS, Harris S (1995) Conifers of Australia’s dry forests
and open woodlands. In: Enright NJ, Hill RS (eds) Ecology of
the southern conifers. Melbourne University Press, Melbourne,
pp 252–270
Bowman DMJS, Panton WJ (1993) Decline of Callitris intratropica
R.T. Baker & H.G. Smith in the Northern Territory: implications
for pre- and post-European colonization fire regimes. J Biogeogr
20: 373–381
Bowman DMJS, Prior LD (2005) Why do evergreen trees dominate
the Australian seasonal tropics? Aust J Bot 53:379–399
Brienen RJW, Zuidema PA (2005) Relating tree growth to rainfall in
Bolivian rain forests: a test for six species using tree ring
analysis. Oecologia 146:1–12
Brodribb TJ, Bowman DJMS, Nichols S, Delzon S, Burlett R (2010)
Xylem function and growth rate interact to determine recovery
rates after exposure to extreme water deficit. New Phytol
188:533–542
Bureau of Meteorology (2010a) Climate data online. http://www.
bom.gov.au/climate/data/index.shtml. Accessed 29 Sept 2010
Bureau of Meteorology (2010b) Australian rainfall and surface
temperature data. http://www.
bom.gov.au/cgi-bin/silo/cli_var/area_timeseries.pl. Accessed 29
Sept 2010
Dulamsuren C, Hauck M, Leuschner C (2010) Recent drought stress
leads to growth reductions in Larix sibirica in the western
Khentey, Mongolia. Glob Change Biol 16:3024–3035
Enquist BJ, Leffler AJ (2001) Long-term tree ring chronologies from
sympatric tropical dry-forest trees: individualistic responses to
climatic variation. J Trop Ecol 17:41–60
Farjon A (2005) A monograph of Cupressaceae and Sciadopitys.
Royal Botanic Gardens, Kew
Fichtler E, Clark DA, Worbes M (2003) Age and long-term growth of
trees in an old-growth tropical rain forest, based on analyses of
tree rings and C-14. Biotropica 35:306–317
Fink D, Hotchkis M, Hua Q, Jacobsen G, Smith AM, Zoppi U, Child
D, Mifsud C, van der Gaast H, Williams A, Williams M (2004)
The ANTARES AMS facility at ANSTO. Nucl Instrum Meth B
223–224:109–115
Fritts HC (2001) Tree rings and climate. The Blackburn Press,
Caldwell
Horne R (1990) Stand height response following variable spacing of
wheatfield white cypress pine regeneration in New South Wales.
Aust For 53:47–54
Hua Q (2009) Radiocarbon: a chronological tool for the recent past.
Quat Geochronol 4:378–390
Hua Q, Barbetti M (2004) Review of tropospheric bomb 14C data for
carbon cycle modeling and age calibration purposes. Radiocarbon 46:1273–1298
123
934
Hua Q, Barbetti M, Worbes M, Head J, Levchenko VA (1999)
Review of radiocarbon data from atmospheric and tree ring
samples for the period 1945–1997 AD. IAWA J 20:261–283
Hua Q, Barbetti M, Zoppi U, Fink D, Watanasak M, Jacobsen GE
(2004) Radiocarbon in tropical tree rings during the Little Ice
Age. Nucl Instrum Method B 223–224:489–494
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of
the Koppen–Geiger climate classification updated. Meteorol Z
15:259–263
La Marche VC, Holmes RL, Dunwiddie PW, Drew LG (1979)
Tree-ring chronologies of the southern hemisphere. Australia
Laboratory of Tree-Ring Research, University of Arizona, Tucson
Lange RT (1965) Growth ring characteristics in an arid zone conifer.
Trans Roy Soc South Aust 89:133–137
Martı́n JA, Esteban LG, de Palacios P, Garcia Fernandez F (2010)
Variation in wood anatomical traits of Pinus sylvestris L.
between Spanish regions of provenance. Trees 24:1017–1028
Pearson S, Hua Q, Allen K, Bowman DJMS (2011) Validating
putatively cross-dated Callitris tree-ring chronologies using
bomb-pulse radiocarbon analysis. Aust J Bot 59:7–17
Pittermann J, Sperry JS, Wheeler JK, Hacke UG, Sikkema EH (2006)
Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant Cell Environ 29:1618–1628
Prior LD, McCaw WL, Grierson PF, Murphy BP, Bowman DMJS
(2011) Population structures of the widespread Australian
conifer Callitris columellaris are a bio-indicator of continental
environmental change. For Ecol Manag. doi:10.1016/j.foreco.
2011.03.030
Reimer P, Reimer RW (2004) CALIBomb radiocarbon calibration.
Interactive program. http://intcal.qub.ac.uk/CALIBomb/frameset.
html. Accessed 10 Dec 2010
Reimer PJ, Brown TA, Reimer RW (2004) Discussion: reporting and
calibration of post-bomb C-14 data. Radiocarbon 46:1299–1304
123
Trees (2011) 25:925–934
Rossi S, Simard S, Rathgeber CBK, Deslauriers A, De Zan C (2009)
Effects of a 20-day-long dry period on cambial and apical
meristem growth in Abies balsamea seedlings. Trees 23:85–93
Rozendaal DMA, Zuidema PA (2011) Dendroecology in the tropics: a
review. Trees 25:3–16
Searson M, Pearson S (2001) A new technique in dendroecology
using Callitris. In: Dargavel J, Hart D, Libbis B (eds) Perfumed
pineries. Environmental history of Australia’s Callitris forests.
Centre for Resource and Environmental Studies, Australian
National University, Canberra, pp 39–47
Sperry JS, Hacke UG, Pittermann J (2006) Size and function in
conifer tracheids and angiosperm vessels. Am J Bot 93:1490–
1500
Stokes MA, Smiley TL (1968) An introduction to tree-ring dating.
University of Chicago Press, Chicago
Vieira S, Trumbore S, Camargo PB, Selhorst D, Chambers JQ,
Higuchi N, Martinelli LA (2005) Slow growth rates of Amazonian trees: consequences for carbon cycling. Proc Natl Acad Sci
USA 102:18502–18507
Walsh RPD, Lawler DM (1981) Rainfall seasonality: description,
spatial patterns and change through time. Weather 36:201–208
Wils THG, Robertson I, Eshetu Z, Sass-Klaassen UGW, Koprowski
M (2009) Periodicity of growth rings in Juniperus procera from
Ethiopia inferred from crossdating and radiocarbon dating.
Dendrochronologia 27:45–58
Wils THG, Robertson I, Eshetu Z, Touchan R, Sass-Klaassen U,
Koprowski M (2011) Crossdating Juniperus procera from North
Gondar, Ethiopia. Trees 25:71–82
Worbes A, Staschel R, Roloff A, Junk WJ (2003) Tree ring analysis
reveals age structure, dynamics and wood production of a natural
forest stand in Cameroon. For Ecol Manag 173:105–123