• Carbon-13 discrimination;
  • drought response;
  • photosynthetic gas exchange;
  • water-use efficiency


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. References

1. The instantaneous and integrated leaf gas exchange of 13 species of southern hemisphere conifers grown under identical glasshouse conditions were examined to determine whether there was any correlation between the characteristics of water use at the leaf level and environmental water availability.

2. In the conifer species examined, the minimum ratio of internal to ambient CO2 measured in leaves during artificially imposed drought [(ci/ca)min] was strongly correlated with the minimum rainfall observed within the natural range of each species. This suggests that the distributions of these species are constrained by the drought tolerance of their photosynthetic apparatus.

3. A good correlation was found between the ratio of internal to ambient CO2 measured in leaves under optimal conditions (ci/ca)max and leaf δ13C (and hence inferred ∫[ci/ca]). Neither of these, however, correlated with the environmental parameters considered most likely to be limiting species distribution, i.e. precipitation and altitude.

4. These data suggest that decreasing water availability may have been the major factor responsible for the restriction and extinction of conifers in the southern hemisphere.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. References

Research into the characteristics and control of leaf gas exchange has been prolific over the last 50 years and the use of leaf photosynthetic characters to explain simple successional changes in the vegetation has become common in the literature, typically using water-use efficiency (e.g. Meinzer, Goldstein & Marisol 1984; Dias-Filho & Dawson 1995), drought response (e.g. Kubiske & Abrams 1993) and light response (e.g. Field 1988; Knapp & Smith 1991; Ashton & Berlyn 1994) to explain small-scale competitive outcomes. This type of eco-physiological research generally takes the form of comparisons between small numbers of species and, as such, does not attempt to make a quantitative link between photosynthetic function and environmental parameters at the larger scale. Indeed, with a few exceptions (e.g. Teeri & Stowe 1976), large-scale relationships between physiology, environment and species distributions have been overlooked by eco-physiologists.

The aim of this study was to determine whether physiological parameters relating to the drought resistance and water use of leaves were related to the water availability within the environmental range of a group of widely distributed conifer species. The physiological character of greatest interest was the maximum instantaneous water-use efficiency during drought, a parameter recently described for leaves of a group of southern hemisphere conifers (Brodribb 1996a). The conifers used in Brodribb (1996a) were shown to produce minimal ‘patchy stomatal closure’ (Terashima et al. 1988) allowing accurate calculation of (ci/ca) during CO2 assimilation. By monitoring ci/ca in drought-stressed plants, the minimum attainable ci/ca could be defined as [(ci/ca)min] for different species. This index was found to be related to the photosynthetic tolerance of these species to low water potential (Brodribb 1996a). The same index was used here on a very similar group of conifers in order to determine whether any correlation existed between drought tolerance and water availability (in terms of minimum average rainfall).

Another signal related to the water-use efficiency of gas exchange (and ci/ca) is the ratio of 12C to 13C in leaves. This character theoretically represents the integrated ratio of ci/ca during CO2 assimilation (Farquhar, Ehleringer & Hubick 1989) and significant correlations have been shown in the relationship between 13C discrimination and instantaneous water-use efficiency (Meinzer, Goldstein & Grantz 1990) and whole plant water-use efficiency (Hubick, Farquhar & Shorter 1986) within species. Thus, carbon-isotope discrimination by leaves has the potential to show spatial trends in gas exchange at a local (Ehleringer et al. 1986; Vitousek, Field & Matson 1990) and global scale (Körner, Farquhar & Roksandic 1988; Körner, Farquhar & Wong 1991; Lloyd & Farquhar 1994), as well as temporal (Marshall & Monserud 1996) and intrageneric (Read & Farquhar 1991) characteristics of leaf gas exchange.

Carbon-isotope discrimination provides an integrated estimate of the ‘intrinsic water-use efficiency’ and is therefore a good compliment to instantaneous gas exchange measurements. Inter-relationships between leaf δ13C, ci/ca and environmental water availability were thus examined in the same conifer species in order to distinguish whether long-term water-use efficiency or photosynthetic tolerance to drought was more important.

The 13 conifer species (from 11 genera) investigated were taken from a diverse geographical range spanning Australia, New Zealand, New Guinea, South Africa and New Caledonia, and a broad spectrum of habitats from the arid zone to tropical rain forest. Species restricted to high (above 3000 m) and low (sea-level) altitudes were also included to ensure that a wide range of leaf morphologies and potential physiological adaptations (Körner & Diemer 1987) were encompassed. These species were considered to be particularly likely to be rainfall limited as there is considerable evidence that the evolution and local extinction of many conifer genera in the southern hemisphere has been strongly influenced by decreasing water availability (Hill 1995).

To ensure that differences recorded between species were species-specific responses rather than being a result of the various local environmental effects encountered in the field, plants were grown and measured under identical conditions.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. References


Cuttings and, where possible, seed were collected from plants in the field, and habitat and altitude descriptions are presented in Table 1. Cuttings of Acmopyle pancheri (Brongn. and Gris) Pilger, Dacrycarpus compactus (Wasscher) de Laubenfels, Diselma archerii Hook.f., Lagarostrobos franklinii (Hook.) C.J.Quinn, Phyllocladus aspleniifolius (Labill.) Hook.f., Podocarpus lawrencii Hook.f. and Microstrobos niphophilus Garden and Johnson, and seed from Actinostrobus acuminatus Parlatore, Athrotaxis selaginoides D.Don, Callitris rhomboidea R.Br., Dacrycarpus dacrydioides (Rich.) de Laubenfels, Podocarpus drouynianus Mueller and Widdringtonia cedarbergensis Marsh, were propagated in sand in Hobart. Upon establishment, all plants were transferred to a pine bark potting mix in 3 litre pots and grown under ambient light conditions in a well-irrigated, heated glasshouse at sea level in Hobart. All species were represented by at least five replicates (and in the case of the cuttings from at least three parent trees), except for A. pancheri, which could only be propagated from two cuttings owing to difficulty in collection (this species is restricted to New Caledonia) and extreme sensitivity to light and humidity conditions during striking.

Table 1.  . Altitude of collection and forest position for the 13 species of conifers investigated during a study of gas-exchange physiology and distribution of conifers Thumbnail image of


Measurement of gas exchange was carried out using the equipment described by Brodribb (1996a). Initially, ci/ca and carboxylation efficiency were measured in fully watered plants photosynthesizing under approximately optimal conditions, with leaves at 20 °C, leaf-air vapour pressure deficit at 5–10mmolmol–1, light intensity at 1400μmol m–2 s–1 and ca = 350±5μmolmol–1. Because the stomatal response of most of the species was very slow, leaves were exposed to full light and 100% relative humidity for a period of 1–2 h prior to measurement of gas exchange to ensure maximum stomatal conductance. For each species, an average of the maximum readings of ci/ca from five individuals was calculated to give (ci/ca)max. Carboxylation efficiency was taken as the initial slope of the A vs ci regression between the CO2 compensation point and ci = 250 μmolmol–1 (Wullschleger 1993). Following determination of maximum rates of gas exchange, water was withheld from plants for a period of 3–4 weeks, during which time ci/ca was regularly measured to determine the minimum attainable ci/ca[(ci/ca)min] under water stress using the technique described by Brodribb (1996a). Except for A. pancheri, values of (ci/ca)min represent averages from five individuals of each species.


Samples of leaf tissue were taken from three glasshouse-grown individuals of each species, ensuring leaves were relatively young, healthy and had developed under completely unshaded conditions. These were then oven dried at 70 °C and ground in a mortice and pestle to a maximum particle size of 0·1 mm. The 13C/12C ratio in this material was assayed (by the Research School of Biological Sciences at the Australian National University in Canberra) and an average and standard error calculated from the three replicates of each species except A. pancheri where only two replicates were available. The relationship between measured δ13C and (ci/ca)max was compared with the theoretical relationship between δ13C and ci/ca, calculated using equation 1 (Farquhar, O’Leary & Berry 1982).

inline image

where δatm is atmospheric 13C ratio relative to PDB standard (– 7·8‰) (Goodman 1980), a is fractionation owing to diffusion (4·4‰) and b is fractionation during carboxylation (net value = 27‰).

A δatm of – 7·8‰ was assumed as plants were grown in a small, well-ventilated glasshouse and were found to have low respiration rates (Brodribb 1996b). The actual value of δatm may have been slightly lower owing to the effects of respiration (Vogel 1993).

Phyllocladus aspleniifolius was included in the discrimination measurements but not in the drought procedure, as it was the only species with multi-veined foliage and hence it could not be ensured that uniform stomatal closure was occurring during drought.


For the reasons stated above, rainfall was the environmental parameter of most interest and because (ci/ca)min appears to reflect drought tolerance (Brodribb 1996a), minimum rainfall figures were considered likely to provide the best correlation.

In attempting to describe the minimum rainfall to which a species is confined, it was necessary to exclude plants that were riparian, or on drainage channels, as these individuals do not rely solely on precipitation for their water supply. Also, estimates were restricted to mature, natural stands of the species in question as information regarding distribution rarely encompasses the scattered, stunted outliers which commonly extend beyond the described limits of a species. Information regarding species distributions was collected either from published material or personal communications and this was used to locate approximately the driest occurrence of each species. It was necessary to show the rainfall estimate for D. dacrydioides as a range, including the driest occurrence for both east- and west-coast populations, because, although the species is present in the dry eastern half of New Zealand, it is invariably riparian or associated with poorly drained soils (P. Wardle, personal communication). Data for other species distributions come from A. pancheri (De Laubenfels 1972), D. compactus (Wade & McVean 1972; Van Royen 1979), A. selaginoides, C. rhomboidea, D. archerii, P. aspleniifolius, P. lawrencii and M. niphophilus (Brown et al. 1983), L. franklinii (Gibson, Davies & Brown 1991), A. acuminatus (Bowman & Harris 1995), P. drouynianus (Gibson et al. 1995) and W. cedarbergensis (Midgley, Bond & Glendenhuys 1995).

Actual rainfall statistics were obtained from the nearest weather station, supplemented in Australia by using estimates from the climatic model BIOCLIM (Nix 1982). Mean monthly rainfall data were used to calculate the mean annual rainfall and minimum average rainfall for the driest four consecutive months (DSR) and in all cases except New Caledonia, rainfall statistics were averages from periods of > 30 years. Four months was used because some of the drier locations experienced a distinctive 4 month block of low rainfall. The New Caledonian data, from Yaté, only represented averages over 2 years.

Because the species used here represented an altitudinal range of 0 to > 3000 m, the influence of altitude of origin on δ13C, ci/ca and carboxylation efficiency was examined to determine whether there was any correlation between measured physiological characters and the large morphological differences observed between alpine and lowland species.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. References

Plants from drier habitats were found to produce lower values of (ci/ca)min (or a higher water-use efficiency) and higher carboxylation efficiencies than species from higher rainfall environments. Of the environmental parameters considered, both yearly average rainfall and rainfall for the dry season (DSR) were significantly correlated with carboxylation efficiency (r2 = 0·85 and 0·82, respectively, with P<0·001 in both cases) and strongly correlated with (ci/ca)min (Fig. 1). Logarithmic regressions provided the best fit for the (ci/ca)min data (r2 = 0·96 for DSR and 0·92 for average rainfall with P < 0·001 in both cases). The x-axis in Fig. 1 shows log10 DSR, and the regression fitted is:


Figure 1. . Minimum ci/ca (or [maximum water-use efficiency]–1) during drought [(ci/ca)min]vs precipitation constraints on the distribution of 12 conifer species. Average rainfall for the four driest consecutive months is shown on a log axis and the logarithmic regression through the data is highly significant (P < 0·001). Phyllocladus asplenifolius has not been included as its broad, multi-veined foliage prevents accurate determination of ci/ca during drought. The precipitation range shown for Dacrycarpus dacrydioides is explained in the text. Species labels for Figs 1 and 2 are: 1, Acmopyle pancheri; 2, Dacrycarpus dacrydioides; 3, Podocarpus lawrencii; 4, Dacrycarpus compactus; 5, Callitris rhomboidaea; 6, Actinostrobos acuminatus; 7, Phyllocladus aspleniifolius; 8, Lagarostrobos franklinii; 9, Microstrobos niphophilis; 10, Athrotaxis selaginoides; 11, Diselma archerii; 12, Podocarpus drouynianus; 13, Widdringtonia cedarbergensis.

Download figure to PowerPoint

inline image

Carboxylation efficiency was related to (ci/ca)min by a simple linear function (r = 0·84, P < 0·001), with high carboxylation efficiencies corresponding to low (ci/ca)min (high maximum water-use efficiency). Neither carboxylation efficiency nor (ci/ca)min, however, showed any relationship to (ci/ca)max.

Mean δ13C values ranged from – 28·95‰ in A. pancheri to – 24·5‰ in P. drouynianus (Table 2). Intra-specific variation in δ13C was generally quite small (< 1·5‰) although the two replicates of A. pancheri produced values of – 27·8‰ and – 30·1‰, resulting in a large standard error. A significant positive correlation (r2 = 0·89, P < 0·001) was found between instantaneous (ci/ca)max and δ13C (Fig. 2) in the 12 species investigated. The regression through the data was almost identical to the theoretical relationship between ci/ca and δ13C calculated from equation 1 (Fig. 2).

Table 2.  . Maximum ci/ca, δ13C, average yearly rainfall and dry season rainfall (driest four consecutive months), for the 13 species of conifers investigated. Some (ci/ca)min data come from Brodribb (1996a) with an increase in replication from three to a minimum of five. The rainfall range shown for D. dacrydioides is explained in the text. * indicates rainfall estimates using the climate model BIOCLIM. Widdringtonia was not included in the δ13C analysis owing to insufficient adult foliage at the time of leaf harvest Thumbnail image of

Figure 2. . Average leaf carbon discrimination (n = 3) and average maximum ci/ca (n = 5) measured at 20 °C, with leaf–air vapour pressure deficit at 5–10 mmolmol–1, light intensity at 1400 μmol m–2 s–1, and c. = 350 ± 5 μmol mol–1 (species labels the same as Fig. 1). Species were grown in a small well-ventilated glasshouse and atmospheric δ13C was assumed to be close to – 7·8‰. The regression through the data (in black) is highly significant (r = 0·89, P < 0·001) and the dotted line represents the theoretical relationship between δ13C and ci/ca using equation 1.

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There was no significant correlation between δ13C and any of the other physiological or environmental parameters investigated [rainfall, (ci/ca)min, carboxylation efficiency] although there was a tendency for species with higher carboxylation efficiencies to produce higher values of δ13C (Table 3). Despite obvious morphological differences between high and low altitude species, i.e. increased leaf thickness and imbricacy in species from high altitude (T. Brodribb & R. S. Hill, personal observations), altitude was not correlated with δ13C or any other physiological character measured.

Table 3.  . Correlation coefficients (r) for regressions between physiological and environmental parameters. All regressions were linear except those indicated Thumbnail image of

Correlation coefficients and significance levels are summarized in Table 3.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. References

The data presented show a good correlation between (ci/ca)min and rainfall parameters in the species investigated, suggesting that the climatic ranges of these conifers is closely controlled by their photosynthetic and gas-exchange characteristics during drought. Although ci/ca measured under uniform, optimal conditions correlated well with leaf δ13C, these leaf characters did not reflect the water availability in the natural range of the conifers studied.


The conifer species investigated produced a large range of leaf δ13C and maximum rates of gas exchange, as would be expected considering the large environmental range represented by these species. Despite this, a good correlation was found between (ci/ca)max and δ13C, indicating that in this group of plants, the long-term water-use efficiency (inferred from δ13C) was well represented by the instantaneous water-use efficiency measured by gas exchange. This result also supports the conclusion that, in these species at least, ci/ca measured by gas exchange gives a reasonable representation of the actual ratio of chloroplast to ambient CO2 concentration. The near-perfect overlap of the theoretical relationship between ci/cavsδ13C and the regression through the measured data (Fig. 2), while aesthetically pleasing, was not expected, considering that bulk leaf material was used and that secondary fractionations are known to occur during leaf metabolism (O’Leary 1981) which would tend to modify the relationship between ci/ca and bulk leaf δ13C (Schleser 1990).

There was no relationship between either (ci/ca)max or δ13C and rainfall parameters, indicating that in these species, water-use efficiency under well-watered conditions does not give any indication of relative drought tolerance exhibited by plants in the field. This refutes the intuitive assumption that plants which produce less negative values of δ13C and high values of instantaneous water-use efficiency are likely to be better adapted to low rainfall and drought (Huc, Ferhi & Guehl 1994). The absence of any correlation between altitude of origin and δ13C was also an unexpected result, as several previous studies have shown significant trends between altitude and δ13C in common garden experiments (e.g. Read & Farquhar 1991; Marshall & Zhang 1994). However, the fact that in these studies altitude of origin has been correlated with both increasing and decreasing δ13C, suggests that altitude may be a secondary effect. The data presented here suggest that the altitude effect has been overridden in this case by the large genetic diversity of the experimental plants.

The lack of correlation between gas-exchange characters measured under optimal conditions and environmental water availability is probably a reflection of the different survival strategies adopted by drought-affected species. Conifer genera such as Callitris, which grow in seasonally dry parts of Australia, have been found to produce relatively indiscriminate water use while water is available, but reduce stomatal conductance to very low levels as soon as soil water potential drops (Atwill & Clayton-Greene 1984).


In contrast to gas exchange measured under optimal conditions, the minimum value of ci/ca (proportional to [maximum water-use efficiency]–1), measured during a slowly intensified drought correlated well with rainfall characteristics at the driest end of the various species ranges. This is an important result as it provides a direct link between instantaneous gas-exchange characteristics and species distribution, further supporting the use of (ci/ca)min as an index of drought tolerance (Brodribb 1996a). This is also emphasized by the fact that a higher correlation was found between DSR than mean annual rainfall (0·96 vs 0·92), as DSR focuses on periods during which the potential for plants to suffer water stress is at its maximum. The logarithmic nature of the regression would be interpreted as reflecting increasing selection for drought tolerance, maximum water-use efficiency, and thus (ci/ca)min, in drier habitats.

Carboxylation efficiency was also correlated with DSR, and although (ci/ca)min and carboxylation efficiency appear to be linked, the production of a high carboxylation efficiency would be of advantage to species growing under conditions of low water availability. Carboxylation efficiency effectively describes the rate of assimilation at different levels of ci (on the linear part of the A vs ci response) and would probably be of increasing importance for plants likely to be operating at lower levels of ci, i.e. plants from drier habitats (Ehleringer & Cooper 1988). This was found to be true in the species investigated here, with increasing environmental aridity correlated with increasing carboxylation efficiency.

Many of the genera used here have well-described fossil histories in Australia and this fossil record provides evidence for a dramatic reduction in conifer diversity and distribution during the Tertiary (Wells & Hill 1989; Hill 1995). Explanations advanced for this decrease in conifer dominance include competitive exclusion by radiating angiosperms, increased disturbance frequency and increasing aridity.

It has been demonstrated that rainfall over much of Australia decreased substantially through the Tertiary (Bowler 1982) and the data presented here add weight to the conclusion that this decrease in the availability of water played an important role in the contraction of conifer forest during this period. First, it shows that these conifers are physiologically limited to minimum rainfall requirements and hence their distribution is likely to be sensitive to changing precipitation characteristics, particularly increasing aridity. Second, the genera shown here to be the most drought sensitive (Dacrycarpus and Acmopyle) were also amongst the first genera to become extinct in Australia, while the more drought-tolerant genera, such as Podocarpus and Callitris, are still quite widespread.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. References
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