Kali B. Middleby1, Lucas A. Cernusak1­, Martin F. Breed2, Darren M. Crayn3,4, Susan G.W. Laurance1, Noel Preece1,5,6, Penny van Oosterzee1,5,6, Jayden Engert1, and Alexander W. Cheesman11 Centre for Tropical Environmental Sustainability Science, James Cook University Nguma-Bada Campus, McGregor Road, Smithfield, QLD, Australia2 College of Science and Engineering, Flinders University, Bedford Park, SA, Australia3 Australian Tropical Herbarium, James Cook University Nguma-Bada Campus, McGregor Road, Smithfield, QLD, Australia4 ARC Centre of Excellence for Indigenous and Environmental Histories and Futures, James Cook University Nguma-Bada Campus, McGregor Road, Smithfield, QLD, Australia5 Biome 5 Pty Ltd., Atherton, QLD, Australia6Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia

AbstractGlobally, the increasing frequency of heatwaves and droughts are impacting tropical forests, which are vital for maintaining biodiversity, carbon sequestration and climate regulation. But vulnerability to warming may vary between and within species due to phenotypic divergence. Leaf functional trait variation is known to affect leaf operating temperatures – a phenomenon termed ‘limited homeothermy’ when it helps avoid lethal temperatures in warmer conditions. Yet, evidence of this purported thermoregulatory ability and the relative roles of acclimation or adaptation remain limited. Here we measured photosynthetic heat tolerance and leaf thermal traits of three, co-occurring tropical rainforest trees across a wide thermal gradient in the Australian Wet Tropics. We used observed leaf traits to predict leaf-to-air temperature differences (∆Ttrait) and combined this with genotypic and environmental data from field collections and glasshouse experiments to assess evidence for intraspecific adaptive selection across the landscape. Intraspecific trait variation led to enhanced leaf cooling (lower or more negative ∆Ttrait) and partial maintenance of modelled thermal safety margins in warmer sites for Darlingia darlingiana and Elaeocarpus grandis, but not Cardwellia sublimis. Genomic signals of selection were detected in all three species, with adaptive genomic variation associated with climate for D. darlingiana and E. grandis, but edaphic factors for C. sublimis. Additionally, E. grandis seedlings from different provenances grown under contrasting temperature and humidity regimes showed clines in ∆Ttrait variation related to mean annual temperature of origin but not treatment environment, despite individual traits acclimating to treatments. Our work implicates local adaptation to climate as a driver of intraspecific variation in leaf thermoregulatory traits, supporting limited homeothermy in these key tropical rainforest tree species. Our results highlight how leaf energy balance modelling can be combined with ecological genomics to better understand the strategies plants use to cope with rising temperatures.

To avoid reaching lethal temperatures during periods of heat stress, plants may acclimate either their biochemical thermal tolerance, or leaf morphological and physiological characteristics to reduce leaf temperature (T leaf). While emerging evidence indicates that plants from warmer environments have a greater capacity to regulate T leaf, the extent of intraspecific variation and contribution of provenance is relatively unexplored. We tested whether upland and lowland provenances of four tropical tree species grown in a common garden differed in their thermal safety margins by measuring leaf thermal traits, midday leaf-to-air temperature differences (∆T leaf), and critical leaf temperature defined by chlorophyll fluorescence (T­ crit). Provenance variation was highly species- and trait- specific. Higher ∆T leaf and T­ crit were observed in the lowland provenance for Terminalia microcarpa, and in the upland provenance for Castanospermum australe, with no provenance differences observed in the other two species. Within-species covariation of T crit and ∆T leaf led to a convergence of thermal safety margins across provenances. These findings suggest that when grown under common conditions, lowland and upland provenances may not differ substantially in their vulnerability (defined here as thermal safety margin) to heat stress, despite differences in operating temperatures and T crit.