Mark J. Hovenden

Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature

In recent years, increased awareness of the potential interactions between rising atmospheric CO2 concentrations ([ CO2 ]) and temperature has illustrated the importance of multifactorial ecosystem manipulation experiments for validating Earth System models. To address the urgent need for increased understanding of responses in multifactorial experiments, this article synthesizes how ecosystem productivity and soil processes respond to combined warming and [ CO2 ] manipulation, and compares it with those obtained in single factor [ CO2 ] and temperature manipulation experiments. Across all combined elevated [ CO2 ] and warming experiments, biomass production and soil respiration were typically enhanced. Responses to the combined treatment were more similar to those in the [ CO2 ]-only treatment than to those in the warming-only treatment. In contrast to warming-only experiments, both the combined and the [ CO2 ]-only treatments elicited larger stimulation of fine root biomass than of aboveground biomass, consistently stimulated soil respiration, and decreased foliar nitrogen (N) concentration. Nonetheless, mineral N availability declined less in the combined treatment than in the [ CO2 ]-only treatment, possibly due to the warming-induced acceleration of decomposition, implying that progressive nitrogen limitation (PNL) may not occur as commonly as anticipated from single factor [ CO2 ] treatment studies. Responses of total plant biomass, especially of aboveground biomass, revealed antagonistic interactions between elevated [ CO2 ] and warming, i.e. the response to the combined treatment was usually less-than-additive. This implies that productivity projections might be overestimated when models are parameterized based on single factor responses. Our results highlight the need for more (and especially more long-term) multifactor manipulation experiments. Because single factor CO2 responses often dominated over warming responses in the combined treatments, our results also suggest that projected responses to future global warming in Earth System models should not be parameterized using single factor warming experiments.

Seasonal not annual rainfall determines grassland biomass response to carbon dioxide

The rising atmospheric concentration of carbon dioxide (CO2) should stimulate ecosystem productivity, but to what extent is highly uncertain, particularly when combined with changing temperature and precipitation. Ecosystem response to CO2 is complicated by biogeochemical feedbacks but must be understood if carbon storage and associated dampening of climate warming are to be predicted. Feedbacks through the hydrological cycle are particularly important and the physiology is well known; elevated CO2 reduces stomatal conductance and increases plant water use efficiency (the amount of water required to produce a unit of plant dry matter). The CO2 response should consequently be strongest when water is limiting; although this has been shown in some experiments, it is absent from many. Here we show that large annual variation in the stimulation of above-ground biomass by elevated CO2 in a mixed C3/C4 temperate grassland can be predicted accurately using seasonal rainfall totals; summer rainfall had a positive effect but autumn and spring rainfall had negative effects on the CO2 response. Thus, the elevated CO2 effect mainly depended upon the balance between summer and autumn/spring rainfall. This is partly because high rainfall during cool, moist seasons leads to nitrogen limitation, reducing or even preventing biomass stimulation by elevated CO2. Importantly, the prediction held whether plots were warmed by 2 °C or left unwarmed, and was similar for C3 plants and total biomass, allowing us to make a powerful generalization about ecosystem responses to elevated CO2. This new insight is particularly valuable because climate projections predict large changes in the timing of rainfall, even where annual totals remain static. Our findings will help resolve apparent differences in the outcomes of CO2 experiments and improve the formulation and interpretation of models that are insensitive to differences in the seasonal effects of rainfall on the CO2 response.

The TasFACE climate-change impacts experiment: design and performance of combined elevated CO2 and temperature enhancement in a native Tasmanian grassland

The potential impacts of climate change on both natural and managed ecosystems are far-reaching and are only beginning to be understood. Here we describe a new experiment that aims to determine the impacts of elevated concentration of CO2 ((CO2)) and elevated temperature on a native Themeda-Austrodanthonia-dominated grassland ecosystem in south-eastern Tasmania. The experimental site contains 60 vascular plant species. The experiment combines the latest developments in free-air CO2 enrichment (FACE) technology with the use of infrared (IR) heaters to mimic environmental conditions expected to exist in the year 2050. The CO2 concentration in the FACE treatments is reliably maintained at 550 µmol mol −1 and leaf temperature is elevated by an average of 2.1 ◦ C by the IR treatment, with 1-cm soil temperature being elevated by 0.8 ◦ C. Measurements being made in the experiment cover plant ecophysiological responses, plant population dynamics and community interactions. Soil processes and ecosystem effects, including nutrient cycling and plant animal interactions, are also being investigated. Collaborations are invited from interested parties.

Altitude of origin influences stomatal conductance and therefore maximum assimilation rate in Southern Beech, Nothofagus cunninghamii

Gas exchange measurements were made on saplings of Southern Beech, Nothofagus cunninghamii (Hook.) Oerst. collected from three altitudes (350, 780 and 1100 m above sea level) and grown in a common glasshouse trial. Plants were grown from cuttings taken 2 years earlier from a number of plants at each altitude in Mt Field National Park, Tasmania. Stomatal density increased with increasing altitude of origin, and stomatal con-ductance and carbon assimilation rate were linearly related across all samples. The altitude of origin influenced thestomatal conductance and therefore carbon assimilation rate, with plants from 780 m having a greater photosynthetic rate than those from 350 m. The intercellular concentration of CO2 as a ratio of external CO2 concentration (ci/ca) was similar in all plants despite the large variation in maximum stomatal conductance. Carboxylation efficiency was greater in plants from 780 m than in plants from 350 m. Altitude of origin has a strong influence on the photo-synthetic performance of N. cunninghamii plants even when grown under controlled conditions, and this influence is expressed in both leaf biochemistry (carboxylation efficiency) and leaf morphology (stomatal density).

Flowering phenology in a species‐rich temperate grassland is sensitive to warming but not elevated CO2

* Flowering is a critical stage in plant life cycles, and changes might alter processes at the species, community and ecosystem levels. Therefore, likely flowering-time responses to global change drivers are needed for predictions of global change impacts on natural and managed ecosystems. * Here, the impact of elevated atmospheric CO2 concentration ([CO2]) (550 micromol mol(-1)) and warming (+2 masculineC) is reported on flowering times in a native, species-rich, temperate grassland in Tasmania, Australia in both 2004 and 2005. * Elevated [CO2] did not affect average time of first flowering in either year, only affecting three out of 23 species. Warming reduced time to first flowering by an average of 19.1 d in 2004, acting on most species, but did not significantly alter flowering time in 2005, which might be related to the timing of rainfall. Elevated [CO2] and warming treatments did not interact on flowering time. * These results show elevated [CO2] did not alter average flowering time or duration in this grassland; neither did it alter the response to warming. Therefore, flowering phenology appears insensitive to increasing [CO2] in this ecosystem, although the response to warming varies between years but can be strong.

Cold-induced photoinhibition and foliar pigment dynamics of Eucalyptus nitens seedlings during establishment

The effects of cold-induced photoinhibition on chlorophyll and carotenoid dynamics and xanthophyll cycling in Eucalyptus nitens (Deane and Maiden) Maiden were assessed between planting and 32 weeks after planting. The seedlings were fertilised or nutrient-deprived (non-fertilised) before planting and shaded or not shaded after planting. The experimental site was 700 m a.s.l., which is considered marginal for establishment of E. nitens plantations in Tasmania due to low mean annual minimum temperatures. Low temperature–high light conditions caused a reduction in variable to maximal chlorophyll fluorescence ratio (F v /F m ), which was more pronounced in non-fertilised than in fertilised seedlings. Shadecloth shelters alleviated this depression. Except in shaded fertilised seedlings, F v /F m did not recover to the level before planting until after 20 weeks. Total chlorophyll content was initially reduced in shaded treatments but subsequently increased with increasing temperatures and F v /F m. Total xanthophyll content and xanthophylls per unit chlorophyll remained relatively constant in fertilised seedlings but decreased in non-fertilised seedlings within 2 weeks after planting. Total xanthophyll and xanthophylls per unit chlorophyll subsequently recovered in non-shaded, non-fertilised seedlings with increasing temperatures and F v /F m. Diurnal [yield and non-photochemical quenching (NPQ) and seasonal (F v /F m) variation in chlorophyll fluorescence parameters were not reflected in xanthophyll cycling during the period of most severe photoinhibition. This result may indicate that chlorophyll–xanthophylls protein complexes form in winter-acclimated E. nitens foliage as have been demonstrated to occur in Eucalyptus pauciflora Sieb. ex Spreng. (Gilmore and Ball 2000, Proceedings of the National Academy of Sciences USA 97, 11098–11101).

Genotypic differences in growth and stomatal morphology of Southern Beech, Nothofagus cunninghamii, exposed to depleted CO2 concentrations

Nothofagus cunninghamii (Hook.) Oerst. clones of four different genotypes from Mt Field National Park, Tasmania were grown at both current (~370 mol mol–1 ) and depleted (~170 mol mol –1 ) CO2. Growth was significantly less in the lower [CO2] treatment in all genotypes. The amount of growth reduction caused by low [CO2] depended strongly upon genotype and varied from less than 30% to greater than 75% reduction of whole plant biomass when compared to growth at current [CO2]. Specific leaf area was significantly greater in all plants grown in reduced [CO2], whereas individual leaf area was not significantly affected by [CO2]. The direction and magnitude of the response of stomatal index, stomatal density and epidermal cell density to [CO2] was strongly dependent upon genotype. [CO2] had a significant effect on the length of the stomatal pore, but the magnitude of the effect (~3%) was trivial compared to changes in stomatal density (up to 20%). There was a significant (P < 0.01) and positive relationship between the response of stomatal density and growth response of a genotype. Therefore, we propose that the response of stomatal density to [CO2] controls the relative growth response of N. cunninghamii and that this response is highly dependent upon genotype.

Strategies of light energy utilisation, dissipation and attenuation in six co-occurring alpine heath species in Tasmania

Alpine environments are characterised by low temperatures and high light intensities. This combination leads to high light stress owing to the imbalance between light energy harvesting and its use in photochemistry. In extreme cases, high light stress can lead to the level of photo-oxidative damage exceeding the rate of repair to the photosynthetic apparatus. Plant species may vary in the mechanisms they use to prevent photodamage, but most comparisons are of geographically and ecologically distinct species. Differences in leaf colouration suggested that photoprotective strategies might differ among Tasmanian evergreen alpine shrub species. We compared chlorophyll fluorescence and leaf pigment composition in six co-occurring alpine shrub species on the summit of Mt Wellington, southern Tasmania, Australia, during spring and autumn. We found marked differences among species in light energy utilisation, attenuation and dissipation. Ozothamnus ledifolius maintained a large capacity for photosynthetic light utilisation and thus, had a low requirement for light dissipation. All five of the other species relied on xanthophyll-cycle-dependent thermal energy dissipation. In addition Epacris serpyllifolia, Richea sprengelioides and Leptospermum rupestre had foliar anthocyanins that would attenuate photosynthetically active light in the leaf. During spring, all species retained de-epoxidised xanthophylls through the night and the pre-dawn concentration of antheraxanthin and zeaxanthin was significantly correlated with reductions in pre-dawn Fv / Fm. We propose that these species use three photoprotective strategies to cope with the combination of high light and low temperature.

Stability of Plant Defensive Traits Among Populations in Two Eucalyptus Species Under Elevated Carbon Dioxide

Plant secondary metabolites (PSMs) mediate a wide range of ecological interactions. Investigating the effect of environment on PSM production is important for our understanding of how plants will adapt to large scale environmental change, and the extended effects on communities and ecosystems. We explored the production of PSMs under elevated atmospheric carbon dioxide ([CO2]) in the species rich, ecologically and commercially important genus Eucalyptus. Seedlings from multiple Eucalyptus globulus and E. pauciflora populations were grown in common glasshouse gardens under elevated or ambient [CO2]. Variation in primary and secondary chemistry was determined as a function of genotype and treatment. There were clear population differences in PSM expression in each species. Elevated [CO2] did not affect concentrations of individual PSMs, total phenolics, condensed tannins or the total oil yield, and there was no population by [CO2] treatment interaction for any traits. Multivariate analysis revealed similar results with significant variation in concentrations of E. pauciflora oil components between populations. A [CO2] treatment effect was detected within populations but no interactions were found between elevated [CO2] and population. These eucalypt seedlings appear to be largely unresponsive to elevated [CO2], indicating stronger genetic than environmental (elevated [CO2]) control of expression of PSMs.

Influence of warming on soil water potential controls seedling mortality in perennial but not annual species in a temperate grassland

In a water-limited system, the following hypotheses are proposed: warming will increase seedling mortality; elevated atmospheric CO2 will reduce seedling mortality by reducing transpiration, thereby increasing soil water availability; and longevity (i.e. whether a species is annual or perennial) will affect the response of a species to global changes. Here, these three hypotheses are tested by assessing the impact of elevated CO2 (550 micromol mol(-1) and warming (+2 degrees C) on seedling emergence, survivorship and establishment in an Australian temperate grassland from autumn 2004 to autumn 2007. Warming impacts on seedling survivorship were dependent upon species longevity. Warming reduced seedling survivorship of perennials through its effects on soil water potential but the seedling survivorship of annuals was reduced to a greater extent than could be accounted for by treatment effects on soil water potential. Elevated CO2 did not significantly affect seedling survivorship in annuals or perennials. These results show that warming will alter recruitment of perennial species by changing soil water potential but will reduce recruitment of annual species independent of any effects on soil moisture. The results also show that exposure to elevated CO2 does not make seedlings more resistant to dry soils.