Current concentrations of O3 in the troposphere pose significant risks to vegetation (Heck, Taylor & Tingey 1988; Lefohn 1992; Fowler et al. 1999; Emberson, Ashmore & Murray 2003). The regional distribution of O3 makes it the most damaging air pollutant globally, for both agricultural and native plant populations. Despite substantial investment in regulatory initiatives and mitigation technologies, O3 exceeds phytotoxic levels in many rural and urban areas, and in both developed and developing countries (Fowler et al. 1999). While O3 is declining in some urban areas, tropospheric O3 is still increasing globally and is projected to do so by up to 1% year−1 for the next half century (Thompson 1992; Stevenson et al. 2000).
Acute O3 exposure (i.e. to relatively high O3) typically leads to visible symptoms, including bronze, deep purple or brown lesions on the adaxial surfaces of exposed leaves (Sandermann 1996; Flagler 1998), as well as to other biological impacts. Chronic exposure to lower concentrations may not lead to visible symptoms, but induces other responses that span the range of scales and levels of biological organization that have been examined. These include changes in gene expression (Sharma & Davis 1994; Miller & McBride 1999; Grimmig et al. 2003), altered growth rates (Laurence et al. 1994), degraded ecosystem function and reduced gene frequency and biodiversity (Taylor, Pitelka & Clegg 1991; Miller & McBride 1999). Visible symptoms have not provided a reliable predictor of these O3 impacts. In loblolly pine (Pinus taeda), for example, independent segregation was observed for O3 tolerance expressed as visible injury or as growth reduction (Taylor 1994) with little correlation between the populations.
Despite decades of investigation (Long & Naidu 2002), neither the biochemical nor the physiological target of O3 attack, the mechanism of ensuing O3 phytotoxicity, nor the key components of plant resistance to O3, have been adequately characterized. This has impeded efforts to predict or model O3 impacts (Massman 2004) and to protect vulnerable crop plants and native vegetation.
Early research into the mechanism of O3 impacts on plants demonstrated that membranes were vulnerable to oxidant attack, with emphasis on plasmalemma and chloroplast membranes and implications for impaired photosynthetic carbon acquisition (Heath 1980). During the same period, evidence accumulated that exposure of foliage to O3 resulted in an accumulation of carbohydrate in the source leaves and reduced translocation to distant sinks (e.g. Hanson & Stewart 1970; Koziol & Jordan 1978). More recently, a compartmental efflux analysis of cotton (Gossypium barbadense) leaves following an acute exposure to O3 indicated that transfer of sugars from the cytoplasm into the phloem was interrupted, providing a potential mechanism for these early observations (Grantz & Farrar 2000).
Reduced allocation of carbohydrate to roots is widely reported, following both experimental exposure to O3 (Oshima, Bennett & Braegelmann 1978; Kasana & Mansfield 1986; Cooley & Manning 1987; Miller 1988; Kostka-Rick & Manning 1992; Laurence et al. 1994; Pell et al. 1994) and across natural exposure gradients (Taylor & Davies 1990; Grulke & Balduman 1999). However, a disturbing level of variability is observed in available literature, even between different O3 exposure experiments using the same plant species. Much of this variability may be related to contrasting environmental conditions and genetic diversity, and some to experimental protocols. Characterizing these effects remains an important goal of future research. A few studies (particularly Reiling & Davison 1992a; Davison & Barnes 1998) have directed attention to reports of unchanged or even increased allocation of carbohydrate to roots following foliar exposure to O3. At present, the generality of O3 impacts on allocation below the ground remains unconfirmed, and is subject to further testing. The physiological and ecological implications of such a general O3 impact are substantial, with significant public policy ramifications. These include quantitative evaluation of carbon sequestration below ground in natural and managed ecosystems, growth and yield forecasts in agricultural and forested systems, predictions of the trajectories of endangered species and development of prescribed management practices for weeds and invasive species that are consistent with changing competitive interactions.
Many reports indicate that O3 exposure alters a specific measure of allocation, the root/shoot biomass ratio, R/S (Wang, Karnosky & Bormann 1986; Cooley & Manning 1987; Chappelka & Chevone 1988; Chappelka, Chevone & Burk 1988; Darrall 1989; Reinert & Ho 1995; Grantz & Yang 1996; Reinert et al. 1996; Dickson et al. 1997; Landolt et al. 1997, 2000; Olszyk & Wise 1997; Chappelka & Samuelson 1998; Franzaring et al. 2000). Unfortunately, R/S and similar allometric relationships such as leaf area per plant mass [leaf area ratio (LAR)] change predictably with plant development (i.e. ontogenetic drift) (Farrar & Gunn 1996; den Hartog et al. 1996) as well as with altered aerial or edaphic environmental conditions (van Noordwijk et al. 1998). O3 may alter the rate of plant development. Thus, accurately determined differences in R/S, sampled at discrete time points, may reflect different points on the growth curves of O3-treated and control plants. This represents a rescaling of the time dimension (van Noordwijk et al. 1998), rather than an altered biological programme of biomass allocation. Exposure of plants to elevated CO2, for example, altered R/S at synchronous harvests without altering allocation (Farrar & Gunn 1996; Poorter & Nagel 2000). A significant treatment effect on R/S neither establishes nor precludes a significant effect on allocation.
The ambiguity of R/S as a measure of allocation may be overcome experimentally in a number of ways (van Noordwijk et al. 1998). Sampling of plants exposed to a range of treatments can be conducted at equivalent developmental stages (i.e. at the same plant size or biomass), rather than at the same plant age (i.e. time point or period after sowing) (Poorter & van der Werf 1998). This approach is less effective if the treatment causes substantial changes in biomass allocation as well as in biomass accumulation.
A more general alternative is offered by an evaluation of an allometric coefficient (k; after Troughton 1955), derived from the exponential growth equation. The planned contrast of k between two environmental treatments explicitly compares the relative growth rates (RGRs) of competing plant parts (Farrar & Gunn 1998; Gunn, Bailey & Farrar 1999). Unlike R/S, allometric coefficients such as k exhibit a nearly constant magnitude over the period of rapid development in plants exposed to unperturbed environments (Troughton 1955; Farrar & Gunn 1998; Gunn et al. 1999; Gunn & Farrar 1999). This enhances the diagnostic value, relaxes the rigid temporal constraints on measurements of biomass ratios and normalizes for treatment differences in growth rates caused by environmental perturbations such as exposure to O3. On a limited basis, an allometric analysis has been applied to the problem of O3 impacts (tabulated data in Table 1). While O3 has been reported to alter R/S in many studies (Cooley & Manning 1987), changes in k have been documented in only a subset (Reiling & Davison 1992a). A rigorous evaluation of the O3 impact on allocation between roots and shoots is required.
|Plant||Stage of growth at initial exposure||Growth/exposure conditions O3||Exposure system||Length of exposure||Reference|
|Thirty-one species||Cotyledon/first leaf stage||< 5 p.p.b.||70 p.p.b.||CEC||7 h d−1 for 2 weeks||Reiling & Davison (1992a)a|
|Five species||4 weeks||16 p.p.b.||71 p.p.b.||CEC||7 h d−1/5 d week−1 for 21 d||Warwick & Taylor (1995)a|
|Three species||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 43 d||Gimeno et al. (2004)a|
|Three species||Seedlings||55 p.p.b.||100 p.p.b.||OTC||Maximum 4 h d−1/5 months year−1 for 3 years||Broadmeadow & Jackson (2000)a|
|Anthyllis cornicina L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 76 d||Gimeno et al. (2004)a|
|Aegilops geniculata Roth||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 64 d||Gimeno et al. (2004)a|
|Aegilops triuncialis L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 65 d||Gimeno et al. (2004)a|
|Avena sterilis L.||4 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 49 d||Gimeno et al. (2004)a|
|Biserrula pelecinus L.||7 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 67 d||Gimeno et al. (2004)a|
|Briza maxima L.||7 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 63 d||Gimeno et al. (2004)a|
|Bromus hordeaceus L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 69 d||Gimeno et al. (2004)a|
|Brassica napus ssp. oleifera var. biennis (oilseed rape), five cultivars||Seedlings||CF||CF + 75 p.p.b.||CEC||6.5 h d−1 for 16 d||Ollerenshaw, Lyons & Barnes (1999)a|
|Calluna vulgaris (summer growth)||Cuttings||CF||70 p.p.b.||OTC||8 h d−1, 5 d week−1 for 24 weeks||Foot et al. (1996)a|
|Citrullus lanatus (watermelon), two cultivars||22-day-old||< 8 p.p.b.||70 p.p.b.||CEC||6 h d−1 for 21 d||Fernandez–Bayon et al. (1993)a|
|Cucumis melo (muskmelon), two cultivars||22-day-old||< 8 p.p.b.||70 p.p.b.||CEC||6 h d−1 for 21 d||Fernandez–Bayon et al. (1993)a|
|Cynosurus echinatus L.||6 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 68 d||Gimeno et al. (2004)a|
|Eucalyptus globulus||Seedlings||4.6 p.p.b.||52.3 p.p.b.||CEC||7 h d−1 for 37 d||Pearson (1995)b|
|Medicago sativa (alfalfa)||4 weeks||CF||60 p.p.b.||GH||6 h d−1/5 d week−1 for 56 d||Cooley & Manning (1988)b|
|Ornithopus compressus L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 47 d||Gimeno et al. (2004)a|
|Picea abies (Norway spruce), two clones||Seedlings||CF||NF||OTC||24 h d−1 for 106 d||Karlsson et al. (1997)b,c|
|Plantago major plants from 22 sites||6-day-old seedlings||< 5 p.p.b.||70 p.p.b.||CEC||7 h d−1 for 14 d||Lyons, Barnes & Davison (1997)a|
|P. major||6-day-old seedlings||< 5 p.p.b.||70 p.p.b.||CEC||7 h d−1 for 14 d||Lyons & Barnes (1998)b|
|P. major, 28 British populations||Cotyledon||< 10 p.p.b.||70 p.p.b.||CEC||7 h d−1 for 14 d||Reiling & Davison (1992b)a|
|Triticum aestivum (spring wheat)||8 d after emergence||< 5 p.p.b.||75 p.p.b.||CEC||7 h d−1 for 30 d||Balaguer et al. (1995)b|
|T. aestivum, two cultivars of spring wheat; three cultivars of winter wheat||Two leaf stage||< 5 p.p.b.||75 p.p.b.||CEC||Maximum 4 h d−1 for 41 d||Barnes, Ollerenshaw & Whitfield (1995)a,d|
|T. aestivum L. cv. Giza 63||25 d after sowing||CF||50 p.p.b.||OTC||10 h d−1/5 d week−1 for 69 d||Hassan (2004)a|
|Trifolium cherleri L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 62 d||Gimeno et al. (2004)a|
|Trifolium glomeratum L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 61 d||Gimeno et al. (2004)a|
|Trifolium striatum L.||6 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 54 d||Gimeno et al. (2004)a|
|Trifolium subterraneum L.||5 weeks||CF||40 p.p.b.||OTC||10 h d−1/5 d week−1 for 66 d||Gimeno et al. (2004)a|
Here, the allocation coefficient, k, and meta-analytical techniques (e.g. Curtis & Wang 1998) are used to evaluate the mean (magnitude) and uncertainty (significance) of O3 impacts on allocation, using information obtained from all available experimental observations. Meta-analytical techniques are becoming frequently used in ecological analyses, most notably for synthesis of the impacts of elevated atmospheric CO2 (e.g. Curtis & Wang 1998; Hedges, Gurevich & Curtis 1999; Wand et al. 1999; Kerstiens 2001; Medlyn et al. 2001; Ainsworth et al. 2002; Wang & Curtis 2002), including a meta-analysis of the impact of elevated CO2 on allocation (Poorter & Nagel 2000). Recently, meta-analytical approaches have been applied to O3 impacts (e.g. on photosynthetic processes in the single species Glycine max) (Morgan, Ainsworth & Long 2003) and on growth responses of tree species (Wittig et al. 2005). The present study provides the first aggregated analysis of available literature on O3 impacts on allocation. The extent to which generalizations regarding O3 impacts on k may be made and the reasons that such generalizations remain problematic are evaluated. A contrast of O3 impacts on k with O3 impacts on plant RGR is provided, as these parameters similarly integrate many O3 effects and similarly facilitate a comparison of O3 effects across diverse species, growth habits, environments and sampling periods. The effects of O3 on k and RGR, documented here by meta-analysis, are contrasted with the effects of shading on k and RGR, from the analysis of Hunt & Cornelissen (1997). Finally, within the constraints of the limited data, O3 effects are contrasted between broad groups of plants and between diverse exposure technologies, to test for effects on the sensitivity of k or RGR to O3.