Barry A. Logan

The seasonal timing and magnitude of photosynthesis in evergreen needleleaf forests (ENFs) has major implications for the carbon cycle and is increasingly sensitive to changing climate. Earlier spring photosynthesis can increase carbon uptake over the growing season or cause early water reserve depletion that leads to premature cessation and increased carbon loss. Determining the start and the end of the growing season in ENFs is challenging due to a lack of field measurements and difficulty in interpreting satellite data, which are impacted by snow and cloud cover, and the pervasive “greenness” of these systems. We combine continuous needle‐scale chlorophyll fluorescence measurements with tower‐based remote sensing and gross primary productivity (GPP) estimates at three ENF sites across a latitudinal gradient (Colorado, Saskatchewan, Alaska) to link physiological changes with remote sensing signals during transition seasons. We derive a theoretical framework for observations of solar‐induced chlorophyll fluorescence (SIF) and solar intensity‐normalized SIF (SIF_relative) under snow‐covered conditions, and show decreased sensitivity compared with reflectance data (~20% reduction in measured SIF vs. ~60% reduction in near‐infrared vegetation index [NIRv] under 50% snow cover). Needle‐scale fluorescence and photochemistry strongly correlated (r² = 0.74 in Colorado, 0.70 in Alaska) and showed good agreement on the timing and magnitude of seasonal transitions. We demonstrate that this can be scaled to the site level with tower‐based estimates of LUE_P and SIF_relative which were well correlated across all sites (r² = 0.70 in Colorado, 0.53 in Saskatchewan, 0.49 in Alaska). These independent, temporally continuous datasets confirm an increase in physiological activity prior to snowmelt across all three evergreen forests. This suggests that data‐driven and process‐based carbon cycle models which assume negligible physiological activity prior to snowmelt are inherently flawed, and underscores the utility of SIF data for tracking phenological events. Our research probes the spectral biology of evergreen forests and highlights spectral methods that can be applied in other ecosystems.

Evergreen needleleaf forests (ENFs) play a sizable role in the global carbon cycle, but the biological and physical controls on ENF carbon cycle feedback loops are poorly understood and difficult to measure. To address this challenge, a growing appreciation for the stress physiology of photosynthesis has inspired emerging techniques designed to detect ENF photosynthetic activity with optical signals. This Overview summarizes how fundamental plant biological and biophysical processes control the fate of photons from leaf to globe, ultimately enabling remote estimates of ENF photosynthesis. We demonstrate this using data across four ENF sites spanning a broad range of environmental conditions and link leaf- and stand-scale observations of photosynthesis (i.e., needle biochemistry and flux towers) with tower- and satellite-based remote sensing. The multidisciplinary nature of this work can serve as a model for the coordination and integration of observations made at multiple scales.

Low temperature in winter depresses rates of photosynthesis, which, in evergreen plants, can exacerbate imbalances between light absorption and photochemical light use. Damage that could result from increased excess light absorption is minimized by the conversion of excitation energy to heat in a process known as energy dissipation, which involves the de-epoxidized carotenoids of the xanthophyll cycle. Overwintering evergreens employ sustained forms of energy dissipation observable even after lengthy periods of dark acclimation. Whereas most studies of photoprotective energy dissipation examine one or a small number of species; here, we measured the levels of sustained thermal energy dissipation of seventy conifer taxa growing outdoors under common-garden conditions at the Red Butte Garden in Salt Lake City, Utah, U.S.A. (forty nine taxa were also sampled for needle pigment content). We observed an extremely wide range of wintertime engagement of sustained energy dissipation; the percentage decrease in dark-acclimated photosystem II quantum efficiency from summer to winter ranged from 6 to 95%. Of the many pigment-based parameters measured, the magnitude of the seasonal decrease in quantum efficiency was most closely associated with the seasonal increase in zeaxanthin content expressed on a total chlorophyll basis, which explained only slightly more than one-third of the variation. We did not find evidence for a consistent wintertime decrease in needle chlorophyll content. Thus, the prevailing mechanism for winter decreases in solar-induced fluorescence emitted by evergreen forests may be decreases in fluorescence quantum yield, and wintertime deployment of sustained energy dissipation likely underlies this effect.

PREMISE: Biological invasions increasingly threaten native biodiversity and ecosystem services. One notable example is the common reed, Phragmites australis, which aggressively invades North American salt marshes. Elevated atmospheric CO₂ and nitrogen pollution enhance its growth and facilitate invasion because P. australis responds more strongly to these enrichments than do native species. We investigated how modifications to stomatal features contribute to strong photosynthetic responses to CO₂ and nitrogen enrichment in P. australis by evaluating stomatal shifts under experimental conditions and relating them to maximal stomatal conductance (g_wmax) and photosynthetic rates.METHODS: Plants were grown in situ in open‐top chambers under ambient and elevated atmospheric CO₂ (eCO₂) and porewater nitrogen (N_enr) in a Chesapeake Bay tidal marsh. We measured light‐saturated carbon assimilation rates (A_sat) and stomatal characteristics, from which we calculated g_wmax and determined whether CO₂ and N_enr altered the relationship between g_wmax and A_sat.RESULTS: eCO₂ and N_enr enhanced both g_wmax and A_sat, but to differing degrees; g_wmax was more strongly influenced by N_enr through increases in stomatal density while A_sat was more strongly stimulated by eCO₂. There was a positive relationship between g_wmax and A_sat that was not modified by eCO₂ or N_enr, individually or in combination.CONCLUSIONS: Changes in stomatal features co‐occur with previously described responses of P. australis to eCO₂ and N_enr. Complementary responses of stomatal length and density to these global change factors may facilitate greater stomatal conductance and carbon gain, contributing to the invasiveness of the introduced lineage.

Summary: Evergreen conifer forests are the most prevalent land cover type in North America. Seasonal changes in the color of evergreen forest canopies have been documented with near‐surface remote sensing, but the physiological mechanisms underlying these changes, and the implications for photosynthetic uptake, have not been fully elucidated. Here, we integrate on‐the‐ground phenological observations, leaf‐level physiological measurements, near surface hyperspectral remote sensing and digital camera imagery, tower‐based CO₂ flux measurements, and a predictive model to simulate seasonal canopy color dynamics. We show that seasonal changes in canopy color occur independently of new leaf production, but track changes in chlorophyll fluorescence, the photochemical reflectance index, and leaf pigmentation. We demonstrate that at winter‐dormant sites, seasonal changes in canopy color can be used to predict the onset of canopy‐level photosynthesis in spring, and its cessation in autumn. Finally, we parameterize a simple temperature‐based model to predict the seasonal cycle of canopy greenness, and we show that the model successfully simulates interannual variation in the timing of changes in canopy color. These results provide mechanistic insight into the factors driving seasonal changes in evergreen canopy color and provide opportunities to monitor and model seasonal variation in photosynthetic activity using color‐based vegetation indices.

The crowns of juvenile Prumnopitys taxifolia (D. Don) de Laub. are comprised of thin, interlaced, wiry stems branching at wide angles and bearing sparse, scale‐like, clasping leaves (‘divaricating’ shoots) that generally surround stems bearing oblong, compressed leaves (‘leafy’ shoots). As development proceeds, non‐divaricating branches of the mature tree form exclusively; thus, P. taxifolia is profoundly heteroblastic. Divaricating stems of juvenile P. taxifolia are brown in appearance and possess very low leaf areas. As such, one might assume that they perform little photosynthesis, returning very little fixed carbon in return for the cost of their construction, and thus represent a significant cost to the overall carbon economy of the whole plant. We examined the hypothesis that divaricating P. taxifolia stems are photosynthetically active, thus mitigating this perceived cost. We found that divaricating shoots, though brown in colouration, possessed chlorophyll contents and capacities for photosynthetic O ₂ evolution on par with those of leafy shoots. Interestingly, measured rates of CO ₂ assimilation in divaricating shoots were only ∼ half those of leafy shoots. This difference may be explained by the assimilation of internal CO ₂ (i.e. CO ₂ generated by or transported through divaricating stems), which is not measured by traditional gas exchange methods. We conclude that analyses of the costs associated with the evolution of divarication or heteroblasty in P. taxifolia should take into account the photosynthetic activity of divaricating stems. A survey of the photosynthetic properties of divaricating stems of other species might contribute to our understanding of the origins and functional significance of this fascinating phenomenon.

Traditional methods of carbon monitoring in mountainous regions are challenged by complex terrain. Recently, solar‐induced fluorescence (SIF) has been found to be an indicator of gross primary production (GPP), and the increased availability of remotely sensed SIF provides an opportunity to estimate GPP across the Western United States. Although the empirical linkage between SIF and GPP is strong, the current mechanistic understanding of this linkage is incomplete and depends upon changes in leaf biochemical processes in which absorbed sunlight leads to photochemistry, heat (via nonphotochemical quenching [NPQ]), fluorescence, or tissue damage. An improved mechanistic understanding is necessary to leverage SIF observations to improve representation of ecosystem processes within land surface models. Here we included an improved fluorescence model within the Community Land Model, Version 4.5 (CLM 4.5), to simulate seasonal changes in SIF at a subalpine forest in Colorado. We found that when the model accounted for sustained NPQ, this provided a larger seasonal change in fluorescence yield leading to simulated SIF that more closely resembled the observed seasonal pattern (Global Ozone Monitoring Experiment‐2 [GOME‐2] satellite platform and a tower‐mounted spectrometer system). We found that an acclimation model based on mean air temperature was a useful predictor for sustained NPQ. Although light intensity was not an important factor for this analysis, it should be considered before applying the sustained NPQ and SIF to other cold climate evergreen biomes. More leaf‐level fluorescence measurements are necessary to better understand the seasonal relationship between sustained and reversible components of NPQ and to what extent that influences SIF.

Northern hemisphere evergreen forests assimilate a significant fraction of global atmospheric CO ₂ but monitoring large-scale changes in gross primary production (GPP) in these systems is challenging. Recent advances in remote sensing allow the detection of solar-induced chlorophyll fluorescence (SIF) emission from vegetation, which has been empirically linked to GPP at large spatial scales. This is particularly important in evergreen forests, where traditional remote-sensing techniques and terrestrial biosphere models fail to reproduce the seasonality of GPP. Here, we examined the mechanistic relationship between SIF retrieved from a canopy spectrometer system and GPP at a winter-dormant conifer forest, which has little seasonal variation in canopy structure, needle chlorophyll content, and absorbed light. Both SIF and GPP track each other in a consistent, dynamic fashion in response to environmental conditions. SIF and GPP are well correlated ( R ² = 0.62–0.92) with an invariant slope over hourly to weekly timescales. Large seasonal variations in SIF yield capture changes in photoprotective pigments and photosystem II operating efficiency associated with winter acclimation, highlighting its unique ability to precisely track the seasonality of photosynthesis. Our results underscore the potential of new satellite-based SIF products (TROPOMI, OCO-2) as proxies for the timing and magnitude of GPP in evergreen forests at an unprecedented spatiotemporal resolution.