A case for the thermal acclimitization of tropical trees

This blog post was heavily inspired by Ken Feeley and his lab exploring temperature effects on tropical tree communities.  see:  http://faculty.fiu.edu/~kfeeley/.  Below:  photo of a typical Neotropical lowland forest. taken at Las Crusas Biological Station in Costa Rica, looking south toward Panama. 

            There is mounting evidence that tropical trees are becoming more and more affected by global climate change, with droughts (1) and increased temperatures becoming more prevalent (2), causing increased tree physiological stress and mortality in tropical forest (3, 4).  The global surface temperature increase by 2100 relative to 1850-1900 is predicted to between 0.3 and 4.8°C, depending on the emissions scenario, with half of the scenarios predicting a >2°C warming (5).  A >2°C warming will affect extensive areas of tropical forests, and there is great uncertainly whether tropical trees will be able to acclimate (6) and how the effects of warming large areas of tropical forest may feedback to affect the earth system (7).  When considering an individual tree, population of individual trees, or communities of tree species, the options are: adapt (i.e., migrate; 8) , acclimate, or go extinct(9).  There is evidence that tropical trees are migrating upslope along elevational profiles in areas where mountains exist (10), resulting in community thermophilization, albeit at low rates, 0.002-0.022 °C year-1 for adult trees(11).  Therefore, the question remains: how will the millions of trees inhabiting the extensive areas of lowland tropical forests (e.g. the Amazon) respond?

            The ability to rapidly and effectively acclimate to the projected increase in the temperature in the tropics has typically be thought of as unlikely(2).  Regardless, using the tenants of classical niche theory in relation to the realized thermal nice, I will entertain three theoretical possibilities of how tropical tree may adapt to climate change.  First, species migration is not needed if niche breath is large, highly plastic, or does not interact directly with the environmental stressor (temperature).  Second, I contend that the underappreciated molecular plasticity in gene expression (i.e. transcriptomic variability) allows species to interact and manipulate their functional niche space in response to an environmental stressor, permitting a large adaptability at evolutionary timescales.  Third, species may acclimate to an environmental stressor if it is spatially or temporally variable, allowing patch dynamics in susceptibility and recovery to drive stress-resistant selection. 

          The evidence that the temperature rise in tropical forest will happen abruptly enough to push tropical trees beyond their physiological limit is mixed, but mounting, and contains some uncertainty (1, 4, 12, 13).  The current ambient air temperature for most tropical evergreen forests lies below 28°C, in some cases well below that mark; areas where air temperatures exceed 28°C tend to support grassland and more-xeric deciduous woody plant communities, in part because these areas are drier(14).  This speaks to the cofounding effects of total precipitation and climate seasonality in understanding temperature responses; mainly, that although the optimal temperature for light saturating photosynthesis for seven tropical forest areas (four Asian and three Amazonian study plots) peaked around 28°C, there was substantial variability among them when accounting for vapor pressure deficit.  Nonetheless, modeled net ecosystem exchange for tropical forests declines above 28°C (14).  Recent work on leaf-level photosynthetic rates of tropical trees shows the optimal temperature for assimilation to be 29°C (15).  Thus, individual trees may be slightly more resistant to temperature increase, than understood when modeling the productivity whole forest s (12).  

         Some of the best, recent evidence suggests that tropical tree species are sensitive to warming, with relative growth and assimilation rates definitely declining above 30°C, and that later successional species with lower photosynthetic capacities being more vulnerable (16).  Slot and Winter (16) grew tree seedlings of three tropical tree species in controlled environments at 25, 30, and 35 °C, and all three species showed some degree of acclimation by increasing their thermal optimum of photosynthesis and reducing respiration rates.  But, increases in thermal optimums of photosynthesis lagged the environmental temperature increase, and rates of photosynthesis still declined significantly in the warmest treatment (with several seedlings dying completely).  Therefore, the thermal niche of tropical trees is somewhat plastic, and species can make physiological adjustments to increasing temperature, up to a point (probably around 30-32°C) (15, 16).  It is unlikely that tropical forest areas will warm fast enough to where such physiological adjustments will not permit the acclimatization by tropical trees; therefore, we can view tropical trees, and tropical forest albeit a bit less so, to have a wide thermal niche.  No doubt, there will likely be stress and mortality of individuals that exist at the edge of the thermal niche(10, 11), for example the warmest locations of the species distribution, or areas undergoing habitat change via increased drought.  Yet, tropical tree species do show physiological adaptability and the overall extinction risk related to thermal stress for tropical forests and most of the species they harbor should remain low.

             Generally, research on the genetic variability in tropical trees has focused on the genomic diversity of trees in space, focusing primarily on their ecological interactions (17).  Analyzing the genomic diversity within communities is undoubtedly one of the major modern biological challenges, and it is becoming increasingly feasible to sequence and assemble transcriptomes (18) and genomes for tropical tree species (19).  Recent transcriptomic evidence using tropical tree communities showed that individual trees can regulate the expression of genes associated the pest and pathogen defense in relation exposure risk (20).  Trees that existed at higher densities with conspecifics had greater levels of gene expression associated with plant defense, showing that negative density dependence operates at both at physiological level via plant-pant interactions and invokes an underlying genetic response.  One can envision this operating with respect to thermal or drought stress, where individuals exposed to the stressor develop an increased ability to respond physiologically via genetic or transcriptomic memory.  In fact, transcriptomic expression by species subjected to experimental drought was a greater predictor of species co-occurrence in space than phylogenetic of functional trait relatedness in a Wisconsin forest (21).  Identifying how gene expression relates to the physiological adaptations of tropical trees subjected to thermal stress is a promising avenue in better understanding the biological processes underlying their responses to increasing temperatures. 

           Lastly, both the physiological (12, 14, 16) and genetic adaptations (20, 21) interact in time and space in a directionally stochastic fashion.  Increased temporal and spatial variability of rainfall and temperature, with the general increasing trend in temperature, are the two main predictions of climate change forecasts(5).  With respect to temperature, I predict persistence in realized niche thermal nice for tropical trees with increased temporal variability in species performance.  Stressful years will increase in frequency and magnitude, but so will years suitable to high performance, and reproduction of tropical trees.  For example high irradiance ENSO years will likely drive forest-wide reproductive bursts in fruit production (22).  If species can adapt physiologically and genetically, at least in the transcriptomic expression of genes associated with physiological adaptation to increased temperature, the logical pathway for evolutionary selection and diversification of species adapted to higher temperatures becomes reasonable.  The patch dynamics (sensu 23) of individual performance, or fitness in relation to thermal stress, and species interactions in space will then determine if tropical trees persist in the coming centuries.  Thus, it becomes increasingly important to maintain large areas of intact tropical forest in well-conserved condition.
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            In conclusion, despite the doomsday rhetoric among some scientific camps and the undeniable facts of anthropogenic climate change, the thermal niche for tropical tree species is broad in most contexts, especially that of the typical lowland tropical forest community.  This allows species to shift within their realized thermal niche, at least with respect to projected temperature increase.  Furthermore, temperature increase. as a stressor. is spatially and temporally variable allowing ample time for physiological and genetic acclimation by species.  Such responses will interact over time and in space to determine the ability of tropical species to evolve in the face of increasing temperatures.  There is evidence that plant communities have responded to climate change in the past (24), yet uncertainty surrounds whether they will continue to do into the future. ♠

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