Testing for temperature acclimation of plant carbon exchange: a comment on ‘Global patterns of the responses of leaf-level photosynthesis and respiration in terrestrial plants to experimental warming’ by Liang et al.

In a recent issue of Journal of Plant Ecology, Liang et al. (2013) use meta-analytical techniques to analyze the leaf carbon exchanges responses to experimental warming and, in part, observe that leaf dark respiration, but not photosynthesis, acclimates to the warming treatments. The authors should be commended for putting together and analyzing such a large data set. Many of the results provide fine syntheses for understanding leaf carbon exchange responses to warming. However, the acclimation analyses are, in my opinion, flawed and are not appropriate for supporting their results.

In short, the authors’ analysis of temperature acclimation involves fitting a regression between the time exposed to warming and the change in leaf carbon exchange (leaf photosynthesis or dark respiration) as a result of warming. Acclimation is then accepted if there is a significant decline in the warming effect over prolonged exposure time. While this analysis may show an interesting and potentially important response, it does not definitively indicate whether acclimation is acting within or across experiments.

Temperature acclimation of plant carbon exchange is a process by which the instantaneous (i.e. seconds to minutes) temperature response of photosynthesis or respiration changes as a result of a long-term (i.e. days to weeks) change in temperature (Armstrong et al. 2008; Atkin et al. 2005; Atkin and Tjoelker 2003; Sage and Kubien 2007; Smith and Dukes 2013; Way and Yamori 2014; Yamori et al. 2014). This response is driven by changes in the basal rate and/or temperature optimum of photosynthetic and respiratory enzymes (Armstrong et al. 2008; Atkin and Tjoelker 2003; Sage and Kubien 2007; Smith and Dukes 2013). Reviews by Way and Yamori (2014) and Atkin and Tjoelker (2003) provide an excellent synthesis of the temperature response and acclimation of photosynthesis and autotrophic respiration, respectively.

Rather than examining changes in instantaneous responses as a result of a growth temperature change within a single species and single experiment, the analysis of Liang et al. (2013) uses average responses across experiments performed for similar time periods. This binning and averaging of responses results in an inability to account for interspecific variation in responses as well as differences in warming magnitude, factors that may be important in this context. For instance, species evolutionarily adapted to acclimate to changes in temperature, such as long lived species and/or species with long leaf lifespan, might possess a greater capacity to acclimate to changes in temperature than species that have not faced similar evolutionary pressures (Atkin et al. 2005; Smith and Dukes 2013).

In addition, as acclimation typically does not result in homeostatic rates of leaf carbon exchange (Atkin and Tjoelker 2003; Kattge and Knorr 2007), the magnitude of warming can have a large impact on observed responses. In fact, while acclimation typically results in dampened process rates in warm grown plants at a common measurement temperature compared to cool grown plants, rates at ambient temperatures, as were assessed in Liang et al. (2013), may be higher, lower or show little difference following acclimation (Atkin and Tjoelker 2003; Way and Yamori 2014).

In their study, Liang et al. (2013) also did not mention whether they controlled for responses of newly developed versus pre-existing leaves. This is an important distinction, as newly developed leaves have a greater ability to acclimate to temperature changes than pre-existing leaves (Campbell et al. 2007). This may have influenced the differences in responses over the wide range of time periods evaluated by Liang et al. (2013).

Finally, many factors, other than acclimation, can influence observed warming responses of leaf carbon exchange to warming including water availability (Joseph et al. 2014), substrate availability for respiration (Atkin and Tjoelker 2003), growth demand (Körner 2013) and vapor pressure deficit (Lin et al. 2012), among others. The influence of these ancillary factors can change over time with warming and need to be accounted for when assessing acclimation responses. A few of these factors are mentioned by Liang et al. (2013), but the fact that they were not taken into account dampens the strength of their conclusions, particularly those regarding acclimation.

Examination of the evidence for temperature acclimation of leaf carbon exchange using large data sets is a fruitful exercise; however, I would advise caution in using this type of analysis. Future studies need to consider mechanisms underpinning acclimation, interspecific and experimental differences, as well as relevant factors that may influence acclimation responses within single studies before comparing across studies. Meta-analyses by Kattge and Knorr (2007) and Way and Yamori (2014) provide excellent examples of how these types of studies could be performed.

FUNDING

N.G.S. recognizes funding from National Aeronautics and Space Administration (NNX13AN65H) and the National Science Foundation (1311358).

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