Root damage by insects reverses the effects of elevated atmospheric CO2 on Eucalypt seedlings.

Scott N Johnson,Markus Riegler,Ben Bond-Lamberty

doi:10.1371/journal.pone.0079479

Abstract

Predicted increases in atmospheric carbon dioxide (CO2) are widely anticipated to increase biomass accumulation by accelerating rates of photosynthesis in many plant taxa. Little, however, is known about how soil-borne plant antagonists might modify the effects of elevated CO2 (eCO2), with root-feeding insects being particularly understudied. Root damage by insects often reduces rates of photosynthesis by disrupting root function and imposing water deficits. These insects therefore have considerable potential for modifying plant responses to eCO2. We investigated how root damage by a soil-dwelling insect (Xylotrupes gideon australicus) modified the responses of Eucalyptus globulus to eCO2. eCO2 increased plant height when E. globulus were 14 weeks old and continued to do so at an accelerated rate compared to those grown at ambient CO2 (aCO2). Plants exposed to root-damaging insects showed a rapid decline in growth rates thereafter. In eCO2, shoot and root biomass increased by 46 and 35%, respectively, in insect-free plants but these effects were arrested when soil-dwelling insects were present so that plants were the same size as those grown at aCO2. Specific leaf mass increased by 29% under eCO2, but at eCO2 root damage caused it to decline by 16%, similar to values seen in plants at aCO2 without root damage. Leaf C:N ratio increased by >30% at eCO2 as a consequence of declining leaf N concentrations, but this change was also moderated by soil insects. Soil insects also reduced leaf water content by 9% at eCO2, which potentially arose through impaired water uptake by the roots. We hypothesise that this may have impaired photosynthetic activity to the extent that observed plant responses to eCO2 no longer occurred. In conclusion, soil-dwelling insects could modify plant responses to eCO2 predicted by climate change plant growth models.

Highlights

Predicted increases in atmospheric carbon dioxide (CO2)concentrations are typically expected to increase plant biomass of C3 plants by 10–20% and C4 plants by 0–10% [1]
While absolute root consumption and removal could not be determined exactly on the basis of differences between infested and control plants, this differences was similar under ambient CO2 (aCO2) and elevated CO2 (eCO2) (910 and 1130 mg in dry mass, respectively) and suggested root consumption was similar
Plant Growth and Biomass Accumulation Plant height was significantly greater for plants grown at eCO2 than those at aCO2 by the time plants were 14 weeks old, which was the case at 16 and 17 weeks (Fig. 1; Table 1)

Summary

Introduction

Background and Rationale Predicted increases in atmospheric carbon dioxide (CO2)concentrations are typically expected to increase plant biomass of C3 plants by 10–20% and C4 plants by 0–10% [1]. Soildwelling insects can be damaging to plant physiology since even minor root damage can: (i) decrease nutrient and water uptake, (ii) cause disproportionate resource losses by severing roots, (iii) divert assimilates belowground for root re-growth and (iv) impair photosynthesis by imposing water deficits [18,19]. This last point may be critical for plant growth responses under eCO2 since increased rates of photosynthesis underpin enhanced growth. This hypothesis is supported by two meta-analyses which reported contrasting effects of above- and belowground herbivores on photosynthesis rates; the former often accelerated photosynthesis rates, potentially to compensate for loss of photosynthetic tissue [20], whereas soil insect herbivores significantly reduced it [19]

Methods

Results

Conclusion