Oecologia (2002) 131:366–374 DOI 10.1007/s00442-002-0905-9
ECOPHYSIOLOGY
C. D. Stylinski · J. A. Gamon · W. C. Oechel
Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species
Received: 15 May 2001 / Accepted: 18 January 2002 / Published online: 21 March 2002 © Springer-Verlag 2002
Abstract This study examined the ability of the Photochemical Reflectance Index (PRI) to track seasonal variations in carotenoid pigments and photosynthetic activity of mature evergreen chaparral shrubs. Our results confirm that PRI scales with photosystem two (PSII) photochemical efficiency across species and seasons, as demonstrated by PRI’s strong correlation with de-epoxidized (photoprotective) xanthophyll cycle pigment levels (normalized to chlorophyll) and with the chlorophyll fluorescence index, ∆F/Fm’. PRI and carotenoid pigment levels (de-epoxidized xanthophyll cycle pigments normalized to chlorophyll or total carotenoid pigments normalized to chlorophyll) were correlated with seasonal fluctuations in midday net CO2 uptake of top-canopy leaves. By contrast, chlorophyll levels (as measured by the Chlorophyll Index) were not as strongly linked to photosynthetic activity, particularly when all species were considered together. Likewise, the Normalized Difference Vegetation Index (NDVI, an index of canopy greenness) did not correlate with net CO2 uptake. Canopy NDVI also did not correlate with canopy PRI, demonstrating that these indices were largely independent over the temporal and spatial scales of this study. Together, these patterns provide evidence for coordinated regulation of carotenoid pigments, PSII electron transport, and carboxylation across seasons and indicate that physiological adjustments are more important than structural ones in modifying CO2fixation capacity during periods of photosynthetic downregulation for these evergreen species. The strong correlation between PRI of whole canopies and PRI of topcanopy leaves suggests that the canopy can be treated as C.D. Stylinski (✉) · W.C. Oechel San Diego State University, San Diego, CA 92182, USA J.A. Gamon California State University, Los Angeles, CA 90032, USA Present address: C.D. Stylinski, University of Maryland Center for Environmental Science, Appalachian Laboratory, 301 Braddock Road, Frostburg, MD 21532–2307, USA, e-mail:
[email protected], Tel.: +1-301-6897272, Fax: +1-301-6897200
a “big leaf” in terms of this reflectance index and that PRI can be used in “scalable” models. This along with the links between carotenoid pigments, PSII photochemical efficiency and carboxylation across species and seasons supports the use of optical assays of pigment levels and PSII activity in CO2 flux models to derive photosynthetic rates. Keywords Carotenoid pigments · Chlorophyll Index · Normalized Difference Vegetation Index · Photochemical Reflectance Index · Xanthophyll cycle pigments
Introduction To understand land-atmosphere carbon fluxes, plant photosynthesis needs to be quantified and monitored over large areas and for long time periods (Field 1991; Ehleringer and Field 1993). Remotely sensed measures of green canopy material, such as the Normalized Difference Vegetation Index (NDVI), are often offered as a rapid, nondestructive and cost-effective means of estimating plant carbon gain over varied spatial and temporal scales (e.g., Field et al. 1995). These indices have been correlated with net primary production (e.g., Goward et al. 1985; Prince 1991) and in some instances with photosynthetic rates (Bartlett et al. 1990; Whiting et al. 1991; Gamon et al. 1993a; Verma et al. 1993; Yoder and Waring 1994; McMichael et al. 1999). However, several studies report that greenness indices do not always scale with photosynthesis, particularly in seasonally dry evergreen ecosystems where canopy greenness remains relatively constant despite significant diurnal and seasonal fluctuations in net CO2 uptake (Running and Nemani 1988; Running and Hunt 1993; Gamon et al. 1995). Reflectance indices derived from narrow-waveband reflectance and responsive to subtle changes in chlorophyll and carotenoid pigments may provide more accurate estimates of seasonal changes in photosynthetic flux of
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evergreen canopies. For example, a narrow-waveband index based on reflectance at 705 and 750 nm has been shown to vary with chlorophyll content during senescence (Gitelson and Merzylak 1994) and early leaf development (Gamon and Surfus 1999) and thus may also indicate seasonally changing chlorophyll content or photosynthetic activity of evergreen plants. Carotenoid pigments of the xanthophyll cycle may also reveal periods of reduced CO2 fixation because they are tied to photochemical efficiency of photosystem two (PSII) (Björkman and Demmig-Adams 1995) and dissipate light energy not used in photosynthesis (Frank et al. 1994). The conversion of these pigments to their de-epoxidized (photoprotective) form alters leaf reflectance in a narrow waveband centered near 531 nm (Gamon et al. 1990, 1993b, 1997). The Photochemical Reflectance Index (PRI) incorporates reflectance at this band and correlates with total content and activity of xanthophyll cycle pigments and with PSII photochemical efficiency of sunlit leaves over diurnal time scales (Gamon et al. 1990, 1997; Peñuelas et al. 1994; Gamon and Surfus 1999; Stylinski et al. 2000). Some studies also report PRI varies with net CO2 uptake or light-use efficiency (Gamon et al. 1992, 1997; Peñuelas et al. 1994, 1995; Filella et al. 1996; Nichol et al. 2000; Rahman et al. 2002), while others found only a weak correlation between these variables for plants under water stress, possibly due to a droughtinduced uncoupling between PSII activity and photosynthetic down-regulation or changes in leaf structure that altered reflectance (Gamon et al. 1992; Peñuelas et al. 1994, 1997). All of these reflectance studies were conducted over short time periods and may not be representative of physiological adjustments that occur over one or more growing seasons. To better understand the relationship between optical indices, plant pigments, and photosynthetic activity over longer time periods, we examined reflectance and physiology of mature field-grown plants measured over two growing seasons. The goals of our study were to investigate (1) seasonal patterns of chlorophyll, xanthophyll cycle pigments and total carotenoid pigments of evergreen Mediterranean-climate chaparral species exposed to seasonal water and temperature extremes and (2) the ability of narrow-waveband reflectance indices measured at the leaf and canopy scales to track seasonal photosynthetic flux of these species. We also examined PRI and pigment levels in the context of the “functional convergence” and “big-leaf” hypotheses described by Field (1991). The functional convergence hypothesis predicts that plants reduce their structural and physiological capacity for CO2 fixation in a coordinated manner when resource limitations prevent efficient exploitation of additional capacity (Field 1991). In the context of our study, we predicted that PSII activity (as measured by PRI) and net CO2 uptake would be regulated in a coordinated manner across seasons, and thus PRI would track seasonal photosynthetic downregulation (we define photosynthetic down-regulation here as a reversible reduction in net CO2 uptake of plants
exposed to unfavorable environmental conditions). The big-leaf hypothesis predicts that the function of leaves and canopies is restricted by similar physical and physiological factors (Field 1991). It has been used to estimate whole-plant stomatal conductance (Jarvis and McNaughton 1986) and photosynthetic rate and capacity (Sellers et al. 1992; Kruijt et al. 1997; Berry et al. 1997) from a single reference value (e.g., a sunlit top-canopy leaf). Based on this hypothesis, we predicted that PRI of leaves in the upper canopy region would vary closely with PRI of whole canopies over multiple seasons.
Materials and methods Study site and species Field measurements were collected in a montane chaparral community near San Diego, California (33° 22′ N, 116° 34′ W). This site is dominated by several evergreen shrub species, including Adenostoma fasciculatum Hook. and Arn., A. sparsifolium Torrey, Ceanothus greggii Gray var. perplexans (Trel.) Jepson, Quercus berberidifolia Liebm. and Arctostaphylos pungens Kunth. Reflectance and physiological measurements were made on mature, healthy individuals of Q. berberidifolia, C. greggii and A. fasciculatum (four to six individuals per species). Plant physiology and reflectance were measured under sunny skies within approximately 2 h of solar noon in March, May/June, July and September/ October 1998 and January, May and July 1999. Measurements were made on fully expanded current-year foliage on terminal shoots. We attempted to standardize light conditions by selecting leaves exposed to saturating sunlight (1,400 to 2,000 µmol m–2 s–1 photosynthetic photon flux density or PPFD) from the top of the canopy or upper portions of the south-facing side (for tall shrubs). Leaf reflectance, fluorescence, and sample collection for pigment analysis were completed at approximately the same time and on the same subset of leaves for each plant. Canopy reflectance, gas exchange, and water potential measurements required more time and equipment and could not be measured concurrently. Instead, most canopy reflectance measurements were collected within 0–4 days of leaf optical measurements (a few measurements were taken 5–11 days after the optical measurements), and photosynthesis and water potential were collected within 1–14 days of optical measurements. All measurements were made under comparable weather conditions with the assumption that midday leaf pigment levels, ∆F/Fm’ and photosynthetic activity would not change markedly with stable weather conditions over this time span. Subsequent studies at this site support this assumption (unpublished data). Pigment content, leaf reflectance and leaf fluorescence were not measured on A. fasciculatum due to time constraints and the difficulty of collecting repeatable reflectance measurements on its narrow short needles (width~1 mm, length
