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Temperate and Tropical Forest Canopies Are Already Functioning Beyond Their Thermal Thresholds for Photosynthesis

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Temperate and Tropical Forest Canopies Are Already Functioning Beyond Their Thermal Thresholds for Photosynthesis Article Temperate and Tropical Forest Canopies are Already Functioning beyond Their Thermal Thresholds for Photosynthesis Alida C. Mau 1, Sasha C. Reed 2, Tana E. Wood 3 and Molly A. Cavaleri 1,* 1 School of Forest Resources & Environmental Science, Michigan Technological University, 1400 Townsend Dr., Houghton, MI 49931, USA; [email protected] 2 U.S. Geological Survey, Southwest Biological Science Center, 2290 S. West Resource Blvd, Moab, UT 84532, USA; [email protected] 3 USDA Forest Service, International Institute of Tropical Forestry, Jardín Botánico Sur, 1201 Calle Ceiba, Río Piedras, PR 00926-1115, USA; [email protected] * Correspondence: [email protected]; Tel.: +970-215-4817 Received: 21 December 2017; Accepted: 15 January 2018; Published: 22 January 2018 Abstract: Tropical tree species have evolved under very narrow temperature ranges compared to temperate forest species. Studies suggest that tropical trees may be more vulnerable to continued warming compared to temperate species, as tropical trees have shown declines in growth and photosynthesis at elevated temperatures. However, regional and global vegetation models lack the data needed to accurately represent such physiological responses to increased temperatures, especially for tropical forests. To address this need, we compared instantaneous photosynthetic temperature responses of mature canopy foliage, leaf temperatures, and air temperatures across vertical canopy gradients in three forest types: tropical wet, tropical moist, and temperate deciduous. Temperatures at which maximum photosynthesis occurred were greater in the tropical forests canopies than the temperate canopy (30 ± 0.3 ◦C vs. 27 ± 0.4 ◦C). However, contrary to expectations that tropical species would be functioning closer to threshold temperatures, photosynthetic temperature optima was exceeded by maximum daily leaf temperatures, resulting in sub-optimal rates of carbon assimilation for much of the day, especially in upper canopy foliage (>10 m). If trees are unable to thermally acclimate to projected elevated temperatures, these forests may shift from net carbon sinks to sources, with potentially dire implications to climate feedbacks and forest community composition. Keywords: forest canopies; tropical forests; photosynthesis; temperature; climate change 1. Introduction Temperate and tropical forests make up much of the world’s biomass, with tropical forests alone accounting for over 60% of terrestrial global carbon [1]. Forests can mitigate the effects of climate change, such as elevated temperature, through carbon dioxide (CO2) uptake during photosynthesis. However, global surface-air temperature is expected to increase by 1 to 5 ◦C by 2100, with an even greater increase expected in northern latitudes, along with an increase in the frequency and intensity of short-term heat waves [2,3]. As temperatures increase, there is a theoretical thermal tipping point after which photosynthesis begins to decline while plant respiration may still be increasing. If declines in CO2 uptake are severe enough that forest-wide respiration exceeds photosynthesis, forests could become net sources of carbon to the atmosphere [4,5]. Determining where this thermal threshold exists and whether different forest types are close to shifting from carbon sources to sinks is crucial to understanding and modeling global climate feedbacks [6]. Many global vegetation models are based on Farquhar’s model of photosynthesis [7], but our ability to accurately parameterize these models is hampered by a lack of mechanistic data on Forests 2018, 9, 47; doi:10.3390/f9010047 www.mdpi.com/journal/forests Forests 2018, 9, x FOR PEER REVIEW 2 of 24 Many global vegetation models are based on Farquhar’s model of photosynthesis [7], but our ability to accurately parameterize these models is hampered by a lack of mechanistic data on Forests 9 physiological2018, , 47 responses to warming and thermal acclimation potential of canopy photosynthesis2 of 24 and respiration, especially for tropical forests [8–16]. Models analyzing the responses of tropical physiologicalcarbon storage responses to elevated to warmingtemperature and have thermal prod acclimationuced inconsistent potential predictions of canopy on photosynthesis whether these andforests respiration, will remain especially sinks or forbecome tropical sources forests [14,17]. [8–16 ].In Modelspart, this analyzing is because the there responses is great ofvariability tropical carbonamong storagetropical to forests elevated in temperatureannual temperature, have produced precipitation, inconsistent soil types, predictions geographic on whether range, these and forestsspecies will assemblage; remain sinks likely or becomeshowing sources a variety [14 ,17of]. re Insponses part, this to ischanging because thereclimate is greatacross variability different amongsystems tropical [18–20]. forests Additionally, in annual temperature,the greatest precipitation,uncertainties soilin model types, geographicprojections range,of global and speciescarbon assemblage;balance over likely the next showing century a variety are for of tropical responses latitu to changingdes, due to climate a combination across different of large systems carbon [18 fluxes–20]. Additionally,and a severe lack the greatestof relevant uncertainties tropical-specific in model data projections [14]. Since tropical of global forests carbon in balanceparticular over account the next for centurysuch a large are forproportion tropical latitudes,of the global due carbon to a combination cycle, any shifts of large in tropical carbon photosynthesis fluxes and a severe could lackalter ofglobal relevant carbon tropical-specific balances and feedbacks data [14]. to Since climate tropical change. forests in particular account for such a large proportionThough of canopy the global warming carbon studies cycle, any will shifts be crucial in tropical in determining photosynthesis whether could different alter global forest carbon types balancescan physiologically and feedbacks acclimate to climate [9,11,14,21–23], change. instantaneous photosynthesis measurements in responseThough to a canopy range of warming temperatures studies are will necessary be crucial to in improve determining models whether and set different a baseline forest to determine types can physiologicallyhow close these acclimate forests are [9 ,to11 ,the14, 21temperature–23], instantaneous optima for photosynthesis photosynthesis. measurements Even in temperate in response forests, to athere range is ofa temperaturesscarcity of data are of necessary the short-term to improve effects models of elevated and set temperatures a baseline to determineon photosynthesis how close in thesemature forests forest are canopies to the temperature and for long-term optima temperature for photosynthesis. acclimation Even [24]. in temperate forests, there is a scarcityLight of datasaturated of the photosynthetic short-term effects response of elevated to temperature temperatures increases on photosynthesis to a maximum in mature (Aopt) forestat an canopiesoptimum and leaf for temperature long-term temperature (Topt), then acclimationdecreases again, [24]. following a parabolic curve (Figure 1) [7,25,26].Light saturated photosynthetic response to temperature increases to a maximum (Aopt) at an optimum leaf temperature (Topt), then decreases again, following a parabolic curve (Figure1)[ 7,25,26]. 9.5 =8.8 µmolCO m-1s-2 9.0 Aopt 2 ) -2 s -1 8.5 m 2 8.0 (µmolCO 7.5 net A 7.0 T = 29°C opt 6.5 20 22 24 26 28 30 32 34 36 38 Temperature (°C) FigureFigure 1. 1.Example Example photosynthetic photosynthetic temperature temperature response response curve from curveDacryodes from excelsa Dacryodes. Photosynthesis excelsa. increasesPhotosynthesis with temperature increases with to a temp thermalerature optimum, to a thermal then rapidlyoptimum, begins then to rapidly decline. begins The temperature to decline. The at maximumtemperature photosynthesis at maximumis photosynthesisTopt, and the photosynthetic is Topt, and the rate photosynthetic at this temperature rate at is thisAopt temperature. is Aopt. Below Topt, photosynthesis typically increases as the rates of biochemical reactions increase Below Topt, photosynthesis typically increases as the rates of biochemical reactions increase with with temperature due to low-temperature limited enzymes [26,27]. In most temperate C3 species, temperature due to low-temperature limited enzymes [26,27]. In most temperate C3 species, photosynthetic decline occurs at leaf temperatures between 26 and 32 ◦C, due to direct biochemical photosynthetic decline occurs at leaf temperatures between 26 and 32 °C, due to direct biochemical limitations and/or to indirect stomatal responses to increases in vapor pressure deficit [7,26]. The two limitations and/or to indirect stomatal responses to increases in vapor pressure deficit [7,26]. The components of net photosynthesis commonly used for model parameterization are the rate of two components of net photosynthesis commonly used for model parameterization are the rate of ribulose-1,5-bisphosphate (RuBP) carboxylation (Vcmax) and the rate of RuBP regeneration from ribulose-1,5-bisphosphate (RuBP) carboxylation (Vcmax) and the rate of RuBP regeneration from the the electron transport chain (Jmax)[7,28]. At elevated leaf temperatures, primary limitations to net electron transport chain (Jmax) [7,28]. At elevated leaf temperatures, primary limitations to net photosynthesis include: temperature sensitivity to Ribulose-1,5-bisphosphate
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