Light use efficiency of California redwood forest understory along a moisture gradient

Louis S. Santiago & Todd E. Dawson

Oecologia

ISSN 0029-8549 Volume 174 Number 2

Oecologia (2014) 174:351-363 DOI 10.1007/s00442-013-2782-9

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Oecologia (2014) 174:351–363 DOI 10.1007/s00442-013-2782-9

Physiological ecology - Original research

Light use efficiency of California redwood forest understory plants along a moisture gradient

Louis S. Santiago · Todd E. Dawson

Received: 6 May 2013 / Accepted: 10 September 2013 / Published online: 26 September 2013 © Springer-Verlag Berlin Heidelberg 2013

Abstract We investigated photosynthesis of five out of five species, coupled with changes in leaf N isotopic species growing in the understory at three sites (1,170-, composition with the onset of the summer fog season sug- 1,600- and 2,100-mm annual moisture inputs), along the gest that natural N deposition increases with rain and fog geographical range of coastal California redwood forest, to inputs and contributes to greater utilization of fluctuating determine whether greater inputs of rain and fog at north- light availability in coastal California redwood forests. ern sites enhance photosynthetic utilization of fluctuating light. Measurements of understory light environment and Keywords community diversity · Fog · Lightfleck · gas exchange were carried out to determine steady state and Nitrogen isotope · Photosynthesis dynamic photosynthetic responses to light. Leaf area index ranged from 4.84 at the 2,100-mm site to 5.98 at the 1,170- mm site. Maximum rates of net photosynthesis and stoma- Introduction tal conductance (g) did not vary appreciably within species across sites. Photosynthetic induction after a change from Light is a critical resource for plants, particularly in for- low to high light was significantly greater in plants growing est understory environments where long periods of low- in lower light conditions regardless of site. Photosynthetic intensity diffuse light are interspersed by brief high- induction also increased with the rate of g in diffuse light, intensity lightflecks. Up to 80 % of the annual C gain in prior to the increase to saturating light levels. Post-illumi- some understory plants occurs during lightflecks (Chaz- nation CO2 assimilation was the largest factor contribut- don 1988). The ability of understory plants to maximize C ing to variation in C gain during simulated lightflecks. The gain during lightflecks depends on: (1) the photosynthetic duration of post-illumination photosynthetic activity, total induction response once a leaf is illuminated, (2) the abil-

CO2 assimilation per light received, and light use efficiency ity to maintain induction during diffuse-light periods, and during simulated lightflecks increased significantly with (3) the ability to continue photosynthetic activity imme- moisture inputs in four out of five species. Increasing leaf diately after a lightfleck (post-illumination CO2 assimila- N concentration with increasing moisture inputs in three tion) (Sharkey et al. 1986; Valladares et al. 1997; Mont- gomery and Givnish 2008). Maximizing C gain may also depend on the overstory canopy structure and its resultant Communicated by Gerardo Avalos. light regime, which determines the temporal distribution of lightflecks, the magnitude of lightflecks, and the total L. S. Santiago · T. E. Dawson amount of light received by an understory plant (Mont- Department of Integrative Biology, University of California, 4007 Valley Life Science Building, Berkeley, CA 94720, USA gomery and Chazdon 2001). Acclimation and adapta- tion to low light therefore involve rapid photosynthetic Present Address: induction in response to sudden increases in light avail- * L. S. Santiago ( ) ability and greater light use efficiency (LUE) than that Botany and Plant Sciences, University of California, 2150 Batchelor Hall, Riverside, CA 92521‑0124, USA expected by steady state CO2 assimilation rates (Chazdon e-mail: [email protected] and Pearcy 1986a, b; Valladares et al. 1997; Montgomery

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352 Oecologia (2014) 174:351–363 and Givnish 2008). Yet, resources besides light might occurrence from June to September, when the lack of also limit the performance of plants in forest understory frontal storms promotes otherwise dry conditions. Indeed environments (Coomes and Grubb 2000). For example, the extent of redwood forest along the California coast nutrient addition has been shown to enhance photosyn- is highly associated with frequency of fog greater than thesis and growth of tropical forest seedlings, even under 40 % (Johnstone and Dawson 2010). Furthermore, there severely low light conditions (Burslem et al. 1996; Pas- is evidence of past declines in abundance of redwood quini and Santiago 2012; Santiago et al. 2012). Further- forests during glaciations (Heusser 1998), when coastal more, initial stomatal conductance (ginitial) is greater and upwelling may have been reduced, thus limiting the fre- photosynthetic induction more rapid during wet season quency of summer fog (Ortiz et al. 1997; Herbert et al. than dry season mornings for tropical understory shrubs, 2001; Johnstone and Dawson 2010). It is also thought illustrating a positive effect of water availability on under- that summer subsidies of fog contribute to the height of story C gain (Allen and Pearcy 2000). To further test the redwood trees through foliar deposition and absorption role of water availability on C gain under low light, we rather than the trees having to always transport water investigated photosynthesis and LUE under fluctuating more than 100 m against gravity (Simonin et al. 2009), light environments across a moisture gradient in Califor- making them the tallest tree species in the world. Conse- nia redwood forest. quently, the shade cast by redwood trees is severe, pro- Ecosystem moisture availability is usually evaluated ducing low light conditions for understory plants (Pfitsch at relatively course scales, often represented across land- and Pearcy 1989a, b). Yet, it is important to understand scapes as annual inputs (Stephenson 1990). However, the ecology of understory plants in redwood forest, the complete suite of water inputs also includes fog, because they represent the largest contribution to plant dew and mist, and other forms of occult precipitation biological diversity of the redwood ecosystem as they (Cavelier and Goldstein 1989; Andrade 2003; Goldsmith grow in the dappled light below a mono-canopy of giants. et al. 2012, 2013), which may provide important sources Recent studies demonstrating that foliar water uptake is of water, especially if they occur during the dry season a common water acquisition strategy for nearly all of the when precipitation is uncommon (Dawson 1998). Occult species that comprise the California redwood forest plant precipitation can be difficult to detect with traditional community (Dawson 1998; Limm et al. 2009), and that micrometeorological techniques such as rain gauges, but the capacity for foliar uptake varies at the landscape scale with prolonged occurrence they can thoroughly saturate within the common redwood forest fern, Polystichum plant canopies and soil, thus substantially increasing munitum (Limm and Dawson 2010), indicate that there plant available moisture (Bruijnzeel et al. 1993; Santiago is large potential for interactions between moisture avail- et al. 2000). Clearly water uptake by roots improves plant ability, foliar absorption and C gain across moisture gra- water status, but for a long time, researchers have known dients in California redwood forest. that water absorption by organs other than roots also Based on better-developed forest understory vegetation occurs (Stone et al. 1950; Stone et al. 1956; Vaadia and at northern redwood forest sites under consistently closed Waisel 1963; Rundel 1982). Under field conditions (Bur- canopy conditions, we expected greater photosynthetic uti- gess and Dawson 2004; Oliveira et al. 2005; Breshears lization of lightflecks in sites receiving greater moisture et al. 2008; Limm et al. 2009; Eller et al. 2013; Gold- inputs. We therefore hypothesized that there were two main smith et al. 2013), as well as in experimental settings ways that moisture inputs could influence the ability of (Simonin et al. 2009), fog interception has been shown to understory plants to exploit fluctuating light. One was that increase plant water status and even photosynthesis, indi- increased moisture promotes greater stomatal aperture in cating that foliar water uptake can enhance plant physi- low light, thus allowing a more rapid induction following ological function and C gain, potentially contributing a sudden increase in light availability. The second was that to greater LUE and a greater C income under low light greater rain and fog would promote soil solution conditions conditions. that favor N uptake, which would have a positive effect Coastal California redwood forests receive moisture on allocation to photosynthetic enzymes such as ribulose- inputs from two main sources: frontal rain storms during 1,5-bisphosphate carboxylase oxygenase and the light- short wet Mediterranean-type winters and summer fog. harvesting complexes of the thylakoid membrane (Evans

Precipitation in redwood forests increases from south to 1989), leading to greater CO2 assimilation per quantity of north, whereas frequency of fog is greatest in northern light received. Moreover, the N in rain, and especially fog California (up to 44 %), and remains high through central (Weathers et al. 2000; Ewing et al. 2009; González et al. California, but declines below 30 % in Oregon and south- 2011), could directly provide greater access to this impor- ern California (Johnstone and Dawson 2010). Impor- tant resource associated with maximizing C gain. Our main tantly, coastal fog peaks in August, with the greatest objectives were to:

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Oecologia (2014) 174:351–363 353

1. examine how steady state and dynamic understory Light environment photosynthesis respond to varying canopy structure across this moisture gradient. Hemispherical photographs were used to quantify the light 2. Determine the consequences of mean annual rain and environment for each plant in which photosynthetic light fog input on the ability of plants in the redwood forest response curves and induction curves were measured. Pho- understory habitat to assimilate C under low light con- tographs were taken using a digital camera (Coolpix 4500; ditions. Nikon, Japan) and a fisheye converter lens (FC-E8; Nikon) 3. Understand how LUE varies with moisture availability with an exposure time of 1/125 and an aperture of 2.8 (Engel- along this environmental gradient. brecht and Herz 2001). The camera was oriented horizontally 15–20 cm above the plant and toward north using a com- pass. All photographs were taken with overcast skies late in Materials and methods the afternoon to maximize contrast between foliage and sky. Estimation of percent direct and diffuse canopy light trans- Study sites and species mittance from hemispherical photographs was accomplished with the Gap Light Analyzer program (Frazer et al. 1999), and This study was conducted at three sites along a 612-km summed to provide total percent canopy light transmittance. north–south gradient along the California coast. This The average canopy cover for each site was measured study region roughly spans the range of the California with a plant canopy analyzer late in the afternoon in Sep- coastal redwood forest, which extends from California’s tember 2005 (LAI-2000; Li-Cor Biosciences, Lincoln, border with Oregon in the northern, high-rainfall end, to NE). Two canopy analyzers that had been inter-calibrated Monterey County at the southern, drier end where forest and synchronized were used for all measurements. One unit begins to grade into chaparral vegetation. The climate was placed in a large clearing for above-canopy measure- of the region is Mediterranean with cool wet winters ments, and the second unit was carried along a 30-m tran- caused by frontal storms, and otherwise dry summers, sect at each site. To minimize the influence of understory except for inputs by coastal summer fog (Dawson 1998). vegetation, LAI-2000 measurements were taken ~1 m We selected three sites over a range of combined mean above the ground (Deblonde et al. 1994). The LAI-2000 annual precipitation and fog inputs of 1,170, 1,600, and measures light using five concentric light-detecting sili- 2,100 mm, with minimal changes in elevation and dis- con rings, sampling five concentric sky sectors with central tance to coast. All sites contain mature forest on flat to zenith angles of 7°, 23°, 38°, 53°, and 68°. We only used moderately sloping (<4°) topography. The 1,170-mm site the first four rings because, due to the tall nature of trees is located along Opal Creek in Big Basin State Park, the in this forest, and rolling hills near the horizon, the 68° 1,600-mm site is located along Bull Creek in Humboldt ring was often not exposed to sky. Leaf area index (LAI) Redwoods State Park, and the 2,100-mm site is located was estimated by an inversion model comparing the trans- on lower Cal Barrel Road in Prairie Creek State Park. mittances, calculated simultaneously for each sky sector, Emergent canopy trees at the sites range from ~75 m at measured above and below the canopy (Cutini et al. 1998). the 1,170-mm site to >110 m at the 1,600- and 2,100- mm sites. Across the 1,170-, 1,600-, and 2,100-mm Community composition sites, interpolated mean annual temperature is 13.1, 10.0 and 11.6 °C, mean relative humidity is 73.3, 74.2, and Plant community composition of the understory was evalu- 74.8 %, mean annual Penman potential evapotranspi- ated in ten 30-m transects with five 0.25-m2 plots randomly ration is 1,068, 863, and 920 mm, and the mean annual chosen along each transect. Within each plot, each individual hours with sunshine is 68.8, 58.5, and 55.1 %, respec- was identified and recorded and a visual assessment of per- tively (New et al. 2002). cent cover was determined. Other species present near tran- To compare photosynthetic C gain of understory plants sects, but not falling in a measurement plot, were recorded for across sites, we selected the five most common understory total species richness per site. Community composition was species across all sites, including saplings ~2 m height of evaluated as plant density, species richness, evenness and the California coast redwood (; dominant Shannon–Wiener Function for diversity (Krebs 1989). canopy tree), and tan oak (Notholithocarpus densiflora; understory to mid-canopy tree), 1- to 2-m-tall huckleberry Photosynthetic light response (Vaccinium ovatum; understory shrub), 5- to 20-cm-tall sor- rel (Oxalis oregana; understory herb) and 0.5- to 1-m tall Photosynthetic CO2 assimilation (A) and g in response western sword fern (Polystichum munitum; fern). We refer to light were measured on newly formed mature under- to all species by generic names hereafter. story leaves from three to four individuals per species

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354 Oecologia (2014) 174:351–363 at each site across a range of photon flux density (PFD; 6 2 1 0–1,000 μmol m− s− ) in July and August 2005. We first Oxalis oregana 2 1 4 measured A at 1,000 μmol m− s− PFD, before light was decreased in a stepwise fashion for a total of ten measure- 2 2 1 ment points to 0 μmol m− s− . Measurements were con- ducted with a portable gas exchange system equipped with 0 an infrared gas analyzer for quantifying precise changes in Notholithocarpus densiflora 4 CO2 and H2O vapor concentrations inside a cuvette con- taining a functional leaf (Li-6400; Li-Cor Biosciences); the 2 cuvette was also outfitted with a red/blue light source (Li-

Cor 6400-02B no. SI-710; Li-Cor Biosciences), with CO ) 2 -1 0 concentration maintained at 400 μmol mol 1, and ambi- s Sequoia sempervirens − -2 ent relative humidity (47.0–73.9 %), and air temperature 4

(16.8–29.0 °C). Parameters for light response curves were mol m µ 2 fit to a non-rectangular hyperbola (Sims and Pearcy 1991). ( are a

A 0 Photosynthetic induction state Polystichum munitum 4 The capacity for understory species to respond to increas- ing PFD, was measured as the time course of A and g after a 2 2 1 step increase in PFD from diffuse levels (10 μmol m− s− ) 0 2 1 to light-saturated levels (300 μmol m− s− ) with the same Vaccinium ovatum portable gas exchange system cited above (Li-6400; Li-Cor 4 Biosciences) in July and August 2005 (Fig. 1). Measure- ments were conducted on leaves that had been acclimated 2 2 1 to ambient light (10–15 μmol m− s− ), but had not been 0 0510 15 20 25 30 35 40 exposed to lightflecks for at least 30 min. ginitial prior to trans- fer from low to high light and the time to reach 90 % of a Time (min) fully induced value of CO2 assimilation (T90) were recorded. Induction state of the leaf is defined as the percent of fully Fig. 1 Representative time course of induction of photosynthetic induced photosynthetic assimilation rate at 60 s since the CO2 assimilation per area (Aarea) of five species growing in the red- time of illumination (A ) (Chazdon and Pearcy 1986a, b). wood forest understory at the 1,170-mm site (Big Basin State Park, 60 CA). Low-light-acclimated leaves experienced 5–10 min of diffuse 2 1 2 1 light (10 μmol m− s− ) before saturating light (300 μmol m− s− ) Lightfleck experiments was applied for 30-45 min

During March and April 2005, photosynthesis during and following short-duration, high-intensity lightflecks was occur if the leaf responded instantaneously to changing light measured with a portable infrared gas analyzer (Li-Cor (Chazdon and Pearcy 1986a, b; Valladares et al. 1997). 6400; Li-Cor Biosciences), by exposing a leaf to diffuse 2 1 light (10 μmol m− s− ) for 5 min, then exposing it to satu- Leaf structure and chemistry 2 1 rating (400 μmol m− s− ) lightflecks of different length (2, 4, 8, 32, 64 s) (Pfitsch and Pearcy 1989a, b). A period of Leaves were collected following photosynthetic measure- 120 s of diffuse light preceded and followed each lightfleck. ments in spring (March and April) and summer (July and

Total A during each lightfleck, post-illuminationC O2 assim- August) 2005, and transported to the laboratory where the ilation (Apost), the duration of post-illumination CO2 fixation leaf area sampled for gas exchange was recorded. Leaves (Tpost), and total CO2 assimilation per PFD received during were dried for 48 h at 65 °C, and weighed for determination the lightfleck and during the post-illumination assimilation of specific leaf area (SLA) so that A could be expressed per period (A/PFD) were calculated. Tpost was defined as the area (Aarea) and per mass (Amass). Dried leaves were ground time for photosynthesis to decrease to within 1 SD of dif- to a fine powder and all leaves from the same individual fuse light values after the step decrease from saturating to plant were pooled for chemical analysis. Leaf C and N diffuse light levels (Fig. 2). LUE was defined as total assimi- concentrations and stable isotopic composition of C (δ13C) 15 lation during the lightfleck (including post-illumination CO2 and N (δ N) were determined with an elemental analyzer fixation) divided by the amount of assimilation that would (ANCA-SL; PDZ Europa Scientific, Manchester, UK),

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500 Table 1 Light environment characteristics in the understory of )

-1 400 coastal California redwood forest sites that vary in annual moisture s

-2 300 inputs

PAR 200 Big Basin State Humboldt Prairie Creek 100 Park (1,170 mm) Redwoods State State Park ( µ mol m 0 Park (1,600 mm) (2,100 mm) )

-1 6

s LAI 5.98 0.10 a 5.58 0.29 a 4.84 0.21 b

-2 4 ± ± ±

area Total transmission (%)

A 2 Notholithocar- 12.5 3.9 a 10.9 1.5 a 13.0 1.4 a 0 ± ± ±

( µ mol m pus densi- -2 flora 0246810 12 Oxalis 11.8 1.3 a 6.0 0.5 a 8.3 0.5 a Time (min) oregana ± ± ± Polystichum 9.8 1.1 a 8.6 3.9 a 10.4 1.2 a Fig. 2 Representative time course of photon flux density (PAR) munitum ± ± ± during lightfleck experiment (upper panel) and response of A to area Sequoia sem- 14.0 2.0 a 5.9 0.6 b 8.4 2.2 b saturating lightflecks (400 μmol m 2 s 1 PAR) of varying duration − − pervirens ± ± ± (lower panel) for a Sequoia sempervirens sapling at the 2,100-mm site (Prairie Creek State Park, CA). Each lightfleck was separated by Vaccinium 13.9 2.2 a 12.3 1.3 a 8.1 1.8 a 2 1 ± ± ± 2-min intervals of diffuse light (10 μmol m− s− ) ovatum Values for total transmission are based on canopy photographs above individual plants (n 3–5). Values for leaf area index (LAI) are based interfaced with a continuous flow isotope ratio mass spec- on site means (n 30).= Values are means 1 SE. LAI values or total = ± trometer (PDZ Europa 20/20; PDZ Europa Scientific), and transmission values within species that do not share the same letter reported in delta notation relative to the Pee Dee belemnite were significantly different (P < 0.05) standard at the Center for Stable Isotope Biogeochemistry. Long-term external precision for the δ13C and δ15N analy- sites than at the 2,100-mm site (Table 1). Despite the great- ses are 0.22 and 0.25 ‰, respectively. est LAI at the 1,170-mm site, the mean canopy light trans- ± mittance of measurement species of 12 % at the 1,170-mm Statistical analysis site was significantly greater than the values of ~9 % at the two wetter sites (P < 0.05), indicating that individuals Data were averaged for each species within a site, and the of these five species grew in slightly higher light environ- average site-specific values for species were analyzed for ments in the driest site. Within species, this difference was variation in light environment, photosynthetic parameters and only significant for Sequoia (Table 1). leaf chemistry as dependent variables. General linear models were used to evaluate variation among dependent variables Community composition with species and sites as categorical independent variables in 2 SAS version 9.2 (SAS Institute, Cary, NC). When significant Mean plant density (individuals m− ) was lowest at the variation was detected, differences among species or sites 1,170-mm site (3.3), peaked at the 1,600-mm site (92.96), were assessed with post hoc Duncan’s multiple range tests. and was intermediate at the 2,100-mm site (68.24; Table 2).

The bivariate relationship between T90 and ginitial was evalu- Mean percent cover increased with increasing moisture ated with non-linear regression in SAS version 9.2 (SAS inputs from 7.4 % at the 1,170-mm site to 31.0 % at the

Institute). The bivariate relationship between A60 and total 1,600-mm site, and 99.6 % at the 2,100-mm site, because canopy transmittance was assessed using standardized major of larger sizes of individuals at the latter. Species rich- axis regression using (S)MATR version 1.0 (Falster et al. ness in measurement plots varied from a low of four at 2003), because both x and y are random variables and x is not the 1,170-mm site, to a high of 15 at the 1,600-mm site, under the control of the experimenter (Sokal and Rohlf 1995). and to 11 at the 2,100-mm site. Total species observed at a site increased with moisture inputs and was 13, 20, and 24 for the 1,170-, 1,600-, and 2,100-mm sites, respectively. Results The Shannon diversity index revealed that diversity was greatest at the 1,600-mm site (1.12), followed by the driest Light environment site (0.76), and lowest at the wettest site (0.43). Evenness, an important component of the Shannon diversity index, The three sites varied in their understory light environment. played an important role in structuring variation in diver- LAI was significantly greater at the 1,170- and 1,600-mm sity across the sites and was greatest at the 1,600-mm site

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Table 2 Density of individuals 2 Species Family Density (individuals m− ) for each California redwood forest understory plant species Big Basin Humboldt Prairie Creek encountered in transects at three Redwoods sites that vary in mean annual moisture inputs (1,170 mm, Big Adenocaulon bicolor Asteraceae 0.32 Basin State Park; 1,600 mm, Anemone deltoidea Ranunculaceae 2.72 0.88 Humboldt Redwoods State Blechnum spicant Polypodiaceae 0.56 Park; 2,100 mm Prairie Creek State Park) Calypso bulbosa Orchidaceae 0.08 Claytonia palustris Portulacaceae 1.12 Dentaria californica Brassicaceae 0.64 Galium spp. Rubiaceae 0.16 hooverianus 1.12 Hierochloe occidentalis Poaceae 1.60 Iris douglasiana Iridaceae 0.32 Notholithocarpus densiflora Fagaceae 0.13 0.32 Oxalis oregana Oxalidaceae 2.53 67.36 62.88 Polystichum munitum Polypodiaceae 0.13 0.80 2.00 Pteridium aquilinum Polypodiaceae 0.16 Rosa gymnocarpa Rosaceae 0.16 Rubus parviflorus Rosaceae 10.24 Smilacina racemosa Convallariaceae 0.16 Trientalis latifolia Primulaceae 0.96 0.56 Trillium ovatum Convallariaceae 0.40 Vaccinium ovatum Ericaceae 0.53 0.24 Vancouveria planipetala Berberidaceae 0.48 Viola sempervirens Violaceae 4.96

2 1 (0.41), followed by the driest site (0.32), with the wettest to 4.35 3.4 mmol m− s− in Polystichum, but was ± site having the lowest evenness (0.18) due to the prevalence not significantly different among species (F 1.35; 4,32 = of Oxalis, which comprised 72 % of all individual plants in P > 0.05). Leaf N (F 112.5; P < 0.0001) and SLA 4,32 = the plots. (F 365.2; P < 0.0001) showed significant variation 4,32 = among species. Photosynthetic leaf traits Photosynthetic induction Among sites, Oxalis was the only species that showed variation in Aarea, with lower values at the wettest site Induction periods during photosynthetic responses to an (F 4.32; P < 0.05; Table 3). There were no significant increase in PFD before steady state photosynthetic rates 2,6 = differences in Amass or maximum g (gmax) within any spe- were reached varied from 5 to 40 min depending on the cies among sites (P > 0.05). Leaf N increased significantly species (Fig. 1). The shape of the response function var- with increasing moisture in Notholithocarpus, Oxalis and ied from a hyperbolic shape in Oxalis, Notholithocarpus, Polystichum, but not in Sequoia or Vaccinium (Table 3). and Polystichum, to a more gradual response in Sequoia

Oxalis was the only species that showed variation in and Vaccinium (Fig. 1). Mean A60 varied from 21 to 56 % SLA among sites, with greater values at the two wetter (43 3 % x¯ 1 SE), and did not differ significantly ± ± sites compared with the driest site (F 7.3; P < 0.05; among species or sites (P > 0.05), but decreased with 2,6 = Table 3). increasing canopy light transmittance (Fig. 3), indicating Across all sites, saplings of the two tree species, that plants growing under lower light availability showed

Sequoia and Notholithocarpus, exhibited greater values of faster induction. T90 was shorter in leaves that had a greater A (F 13.4; P < 0.0001) and A (F 77.5, g (Fig. 4), and was significantly lower at the 1,600- area 4,32 = mass 4,32 = initial P < 0.0001), than the low-statured species, Oxalis, Poly- mm site (9.1 2.4 min) compared to the 1,170-mm site ± stichum, and Vaccinium. Mean gmax across species var- (14.3 1.9 min) and the 2,100-mm site (15.3 1.9 min) 2 1 ± ± ied from 67.5 11.8 mmol m− s− in Notholithocarpus (F 4.61; P < 0.05). Values for g were not ± 2,26 = initial 1 3 Author's personal copy

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Table 3 Maximum stomatal Big Basin State Humboldt Redwoods Prairie Creek State conductance (gmax), maximum Park (1,170 mm) State Park (1,600 mm) Park (2,100 mm) photosynthetic CO2 assimilation rate per area (A ), maximum 2 1 area gmax (mmol m− s− ) photosynthetic CO assimilation 2 N. densiflora 50.9 10.2 a 83.8 29.9 a 67.8 28.4 a rate per mass (Amass), leaf N ± ± ± O. oregana 78.5 16.2 a 53.5 14.8 a 44.7 6.5 a concentration, and specific ± ± ± leaf area (SLA) for five species P. munitum 48.7 2.8 a 44.2 10.4 a 35.8 6.0 a ± ± ± studied along a moisture S. sempervirens 52.0 7.6 a 49.9 1.1 a 59.7 1.6 a gradient in coastal redwood ± ± ± forest in California, USA V. ovatum 35.0 10.7 a 71.7 45.5 a 43.4 15.5 a 2 1 ± ± ± Aarea (μmol m− s− ) N. densiflora 4.6 0.4 a 5.5 0.8 a 5.4 0.7 a ± ± ± O. oregana 4.5 0.3 a 3.4 0.2 ab 3.1 0.2 b ± ± ± P. munitum 3.9 0.1 a 3.5 0.3 a 3.2 0.2 a ± ± ± S. sempervirens 5.0 0.7 a 5.0 0.3 a 5.5 0.1 a ± ± ± V. ovatum 3.1 0.7 a 3.3 0.1 a 3.1 0.9 a 1 1 ± ± ± Amass (nmol g− s− ) N. densiflora 45.0 2.2 a 62.7 8.6 a 62.0 21.3 a ± ± ± O. oregana 201.2 28.0 a 193.5 15.5 a 165.5 6.6 a ± ± ± P. munitum 63.1 6.3 a 66.2 5.4 a 58.1 6.3 a ± ± ± S. sempervirens 41.3 7.6 a 41.1 0.6 a 46.8 0.7 a ± ± ± V. ovatum 44.1 12.8 a 32.0 1.1 a 40.3 16.3 a 1 ± ± ± Leaf N (mg g− ) N. densiflora 9.3 0.0 a 10.6 0.8 a 13.0 1.2 b ± ± ± O. oregana 19.7 0.5 a 24.2 2.0 b 22.9 1.6 ab ± ± ± P. munitum 12.6 0.1 a 13.9 0.2 b 15.1 0.5 c ± ± ± S. sempervirens 7.1 0.9 a 7.9 0.8 a 9.0 1.4 a ± ± ± V. ovatum 9.9 1.4 a 8.2 0.8 a 9.7 1.0 a 2 1 ± ± ± SLA (cm g− ) N. densiflora 99.0 7.7 a 113.7 4.0 a 110.8 23.0 a Values are mean 1 SE for ± ± ± ± O. oregana 442.6 35.7 a 570.2 10.1 b 534.8 24.9 b three to five individuals per site. ± ± ± Values with different letters P. munitum 162.5 13.5 a 189.5 16.1 a 180.1 9.7 a ± ± ± within the same species are S. sempervirens 82.7 7.4 a 82.4 3.4 a 85.8 0.2 a ± ± ± significantly different (ANOVA, V. ovatum 134.5 17.0 a 97.2 0.3 a 125.4 15.4 a P < 0.05) ± ± ±

significantly different among sites (P > 0.05), but among Among species, there were large differences in Tpost with species, they were significantly greater for Notholithocar- Polystichum showing the longest mean T of 25.1 0.7 s post ± pus than Sequoia and Vaccinium, with Oxalis and Polysti- and Oxalis showing the shortest of 17.9 0.6 s, and other ± chum showing intermediate values (F 2.91; P < 0.05). species exhibiting intermediate values (F 10.0; 4,31 = 4,232 = P < 0.0001; Fig. 5). Apost averaged across lightflecks of dif- Lightfleck experiments ferent length increased with increasing moisture inputs and was significantly greatest at the 2,100-mm site, intermediate

Mean photosynthetic CO2 assimilation during illumination in at the 1,600-mm site, and significantly lower at the 1,170- 2 experimental lightflecks ranged from 6.15 0.37 μmol m− mm site (F2,232 18.6; P < 0.0001; Fig. 5). A/PFD was sig- ± 2 = during 2-s lightflecks to 164.45 9.38 μmol m− during nificantly greater at the 2,100- and 1,600-mm sites compared ± 64-s lightflecks. Mean T for all lightflecks was 22.3 s to the 1,170-mm site (F 3.74; P < 0.05; Fig. 5). The post 2,232 = and thus Apost contributed 11–94 % of total C gain caused one species that showed an exception to the general statisti- by experimental lightflecks. There was no significant vari- cal trend of increasing Tpost, Apost, and A/PFD with increasing ation among sites in the amount of CO assimilated during moisture was Oxalis, which caused significant site spe- 2 × illumination in lightfleck experiments (P > 0.05). How- cies interactions in these three variables (P < 0.05; Fig. 5). ever, T was greater at the 2,100-mm site (26.1 0.9 s) The total amount of CO assimilation caused by experimen- post ± 2 than at the 1,170- and 1,600-mm sites (20.0 0.6 and tal lightflecks was significantly related to T for all light- ± post 21.7 0.6 s, respectively; F 23.5; P < 0.0001; Fig. 5). fleck lengths (Fig. 6). This relationship was strongest for 2-s ± 2,232 = 1 3 Author's personal copy

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65 35

60 Notholithocarpus Oxalis 30 55 Polystichum Sequoia 50 25 Vaccinium 45

40 20 assimilation (s) 2 35 2 initial illumination (%) r = 0.40 15 CO 30 Time of post-illumination Induction state 60 seconds after 25 10 46810 12 14 16 Canopy light transmittance (%) ) 50 2 -2

Fig. 3 Induction state as a function of canopy light transmittance for five species of redwood forest plants growing in the understory [Not- mol m 40 holithocarpus densiflora (inverted triangles), Oxalis oregana (trian- µ gles), Polystichum munitum (diamonds), Sequoia sempervirens (cir- 30 cles), Vaccinium ovatum (squares)]. Each point represents the mean of each species at one of three sites along a moisture input gradient. Solid symbols Plants from the 2,100-mm site, gray symbols plants 20 Post illumination CO from the 1,600-mm site, open symbols plants from the 1,170-mm site. assimilation ( Leaf induction state was calculated as the percent of maximum pho- tosynthetic rate reached after 60 s of exposure to high light follow- 10 ing 5–10 min in diffuse light. The line represents the best-fit standard major axis regression line (y 3.22x 77.6; P 0.01) ) = − + = -1 25

20 40

2 mol photon s r = 0.65 2 15 30

Assimilation per PF D 10 (mmol CO 20 (min)

90 5 T 1170 1600 2100

10 Mean annual moisture inputs (mm)

0 Fig. 5 Mean time of post-illumination CO2 assimilation (upper 10 20 30 40 50 60 panel), mean post-illumination CO2 assimilation (middle panel), and -2 -1 total assimilation caused by lightfleck per unit PFD received dur- Initial conductance (mmol H2O m s ) ing the lightfleck and the post-illumination CO2 assimilation period (lower panel), for five species of redwood forest understory plants Fig. 4 Time to reach 90 % of maximum photosynthetic rate after from three sites along a moisture input gradient illumination with high light (T90) as a function of initial stomatal con- ductance of the leaf under diffuse light prior to exposure to high light (ginitial). Points are means 1 SE. Symbols as in Fig. 3. The fitted line ± ( 0.113x) ( 0.0000000000327x) values (F 4.09; P < 0.005). LUE decreased with represents the equation y 47.4e − 8.56e − 2,232 = = + increasing lightfleck duration in all species (Fig. 7). These leaves which were induced by diffuse light, exhibited LUEs lightflecks, and the strength of this relationship decreased as high as 800 % for 2-s lightflecks (Fig. 7). with increasing lightfleck length (Fig. 6). Mean LUE across species also increased with increasing Leaf stable isotopic composition moisture inputs and was significantly greater at the 2,100- mm site (277 28 %) than at the 1,170-mm site (177 16), Leaf δ13C across species was significantly greater at the ± ± with the 1,600-mm site (226 20 %) showing intermediate 2,100-mm site ( 32.5 ‰) than at the 1,600-mm ( 33.1 ‰) ± − − 1 3 Author's personal copy

Oecologia (2014) 174:351–363 359

sites in the March–April rainy season (F 16.28; 2 s 2,58 = 40 P < 0.0001) and during the July–August fog season (F 16.74; P < 0.0001; Fig. 8). The wettest site also 2,53 = 30 produced an appreciable change in δ15N with the onset of the summer fog season, as δ15N dropped precipitously, 20 whereas in the two drier sites, the change from the spring r 2 = 0.59 rainy season to the summer fog season was within the SE of the zero value (Fig. 8). 4 s 60 Discussion 40 )

-2 We tested the ability of plants in the redwood forest under- 20 2 r = 0.44 story to assimilate CO2 in constant and fluctuating light in response to a gradient of moisture inputs. Our data demonstrate that overall, understory plants conduct post- 70 8 s illumination CO2 fixation for a longer time (greater Tpost), 60 show greater A during the post-illumination period (greater 50 Apost), and obtain more CO2 per total light received during 40 experimental lightflecks (greaterA /PFD), with increasing moisture inputs. Our data also indicate that greater g at the 30 r 2 = 0.35 onset of photosynthetic induction (ginitial) reduces the time to reach 90 % of the fully induced value of CO2 assimi- 140 32 s lation (T90) following transfer from low to high light. Fur-

Assimilation due to lightfleck ( µ mol m 120 thermore, increasing LUE with increasing moisture inputs 100 integrates the importance of departures from steady state photosynthetic light responses and highlights the extent to 80 which post-illumination CO2 fixation can be important in 60 r 2 = 0.20 maximizing C gain in an environment where both water and light can be limiting. However, we did not find evi- 400 dence that plants in wetter sites showed greater induction 64 s state measured as the percent of fully induced photosyn- 300 thetic assimilation rate 60 s after illumination (A60). Thus, 200 our data indicate that C gain during short-duration light- flecks increases with moisture inputs along the range of 100 r 2 = 0.24 California redwood forests and is consistent with two out of three of the well-known ways in which plants are known 10 15 20 25 30 35 40 to maximize C gain in low light (Sharkey et al. 1986; Val- Time of post-illumination CO2 fixation (s) ladares et al. 1997; Montgomery and Givnish 2008). Our data are also consistent with increased understory C gain

Fig. 6 Total CO2 assimilation caused by lightfleck during illumina- as a mechanism enhancing greater understory plant density tion and during the post-illumination CO2 assimilation period as a and percent cover in northern high-moisture sites relative to function of the time of post-illumination CO2 assimilation activity drier southern sites across the span of California redwood for five species of redwood forest understory plants from three sites along a moisture input gradient. The panels reflect lightflecks of dif- forest. ferent duration from 2 to 64 s. Symbols as in Fig. 3. Lines represent Although our data indicate significant increases in Tpost, the best-fit standard major axis regression line (2 s y 2.10x 9.99, = − Apost and A/PFD with increasing moisture inputs across this P < 0.001; 4 s y 2.15x 7.28, P < 0.01; 8 s y 2.84x 13.5, gradient when all species are considered, the response of P < 0.05; 32 s y = 4.34x − 8.24, P < 0.1; 64 s y = 12.4x−64.7, P 0.05) = + = − Oxalis was strikingly different (Fig. 5). In contrast to the = other four species which show a pattern of increasing post-

illumination CO2 fixation with increasing moisture, val- and 1,170-mm ( 33.3 ‰) sites (F 5.49; P < 0.01), ues of T , A and A/PFD in Oxalis actually decreased − 2,58 = post post although the total range of values was small. Leaf δ15N with moisture inputs. These counterintuitive results are decreased significantly with increasing moisture among likely caused by the low stature of Oxalis (<20 cm), and

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1 Notholithocarpus densiflora 800 Winter rain season 1170 mm 0 600 1600 mm 2100 mm A B C 400 -1 200 -2

Oxalis oregana 800 -3 Summer fog season 600 0

400 N (‰) ABC 15 δ 200 -1

-2 Polystichum munitum 800 -3 600

400 0 200 N (‰) 15 δ

Light use efficiency (%) -1 Sequoia sempervirens 800 Change in 600 -2 400 BB HR PC

200 Fig. 8 Site means ( 1 SE) of five species of redwood forest under- story plants for leaf± N isotopic composition (δ15N) measured during spring and summer, and the difference between seasons. Means with Vaccinium ovatum different letters are significantly different at P 0.05. BB Big Basin 800 State Park, HR Humboldt Redwoods State Park,≤ PC Prairie Creek State Park 600

400 supporting the notion that moisture enhances the ability 200 of this species to thrive in low light. Interestingly, Oxalis shows the lowest amount of foliar water uptake among ten 110 100 common redwood forest plant species (Limm et al. 2009), Lightfleck length (s) suggesting that Oxalis is highly dependent on soil water uptake in order to maintain stomatal apertures that mini-

Fig. 7 Light use efficiency as a function of lightfleck duration (log mize T90. These data are also consistent with the findings scale) of induced leaves for five species of redwood forest understory of Pfitsch and Pearcy (Pfitsch and Pearcy 1989a, b), whose plants from three sites along a moisture input gradient (1,170, 1,600 1 work on Adenocaulon bicolor demonstrates the importance and 2,100 mm year− ). Solid symbols Plants from the 2,100-mm site, gray symbols plants from the 1,600-mm site, open symbols plants of ginitial and rapid photosynthetic induction (Oxalis; Fig. 1) from the 1,170-mm site. Points are mean 1 SE for maximizing C gain in the redwood forest understory ± environment. Our data also indicate that although understory veg- the progressively increasing vegetation cover as moisture etation density and cover increase with moisture inputs, inputs increase toward northern humid sites. This find- canopy coverage did not vary substantially and was actu- ing is relevant because although Oxalis individuals appear ally slightly lower at the 2,100-mm site. This difference to become increasingly shaded at wetter sites, they also is likely due to the immense size of trees at the 2,100-mm increase in abundance with moisture inputs (Table 2), site, which have a strong effect on canopy structure and

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Oecologia (2014) 174:351–363 361 light transmittance. The large vertical orientation and mini- 2000; Ewing et al. 2009; González et al. 2011), greater mal branching low in the canopy of the giant trees along inputs of rain and fog at wetter sites may simply repre- Cal Barrel Road at the 2,100-mm site (Sawyer et al. 2000), sent an increase in plant available N inputs. The timing of transmit light to the understory in a manner that may be seasonal change in foliar δ15N at the 2,100-mm site corre- better described as “sun swaths” rather than sunflecks sponds to the change from spring frontal rains to summer (L. S. Santiago, personal observation). Canopy light condi- fog, suggesting that the shift in foliar δ15N corresponds tions may also be associated with greater foliar δ13C values to a change in source N. A 5-year study in redwood for- at the 2,100-mm site compared to the two drier sites, con- est in the middle of the redwood range shows that most sistent with reports of increasing δ13C values of Redwood dissolved inorganic N is delivered to the forest floor as forest understory plants with increasing daily PFD (Pearcy NO3−, and that forest throughfall N is seven times greater and Pfitsch 1991), as well as other studies demonstrat- during the fog season compared to the rain season (Ewing ing greater δ13C values with increasing light availability et al. 2009), consistent with the possibility that the (Ehleringer et al. 1987; Zimmerman and Ehleringer 1990). change in foliar δ15N with the onset of the fog season at However, Pearcy and Pfitsch (1991) show δ13C variation of the foggiest site represents a shift to fog-based N forms. over 3 ‰, whereas our complete variation is 0.8 ‰ and our Furthermore, at the same site as the Ewing et al. (2009) 15 values are in a range suggesting influence by respired CO2 study, δ N of fog NO3− was not significantly different from soil, which is always more negative than source air from rain ( 1.2 0.68 ‰), but δ15N of NH in through- − ± 3 (Sternberg et al. 1989; Buchmann et al. 1997), thus limiting fall ( 3.37 0.69 ‰) was more depleted than in fog + ± our ability to place too much emphasis on the physiologi- ( 10.04 1.56 ‰) (Templer et al. 2006), also supporting + ± cal implications of these values. Furthermore, understory the idea that foliar δ15N changes with the arrival of fog light conditions represent a combination of canopy light signify a shift to fog-based N forms. Preliminary data col- interception and sky conditions, and the 2,100-mm site lected at the 2,100-mm site show that mean δ15N of two receives approximately 12 % fewer hours of sunshine than samples of August 2005 fog NO − ( 1.7 ‰) was more 3 − the 1,170-mm site (New et al. 2002), as well as a greater depleted than one sample of March 2005 rain ( 4.4 ‰; + frequency of fog (Johnstone and Dawson 2010). Therefore, L. S. Santiago, unpublished data), consistent with the lower light conditions likely prevail with increasing north- depletion in foliar N at this site at the onset of the summer ern exposure along this gradient, even though individual fog season. However, there simply are not enough data plants can show substantial variation in terms of their loca- on δ15N of fog N to confirm whether the seasonal shift tion and light habitats in the heterogeneous forest under- in foliar δ15N at the 2,100-mm site is caused by a shift of story, making it difficult to distinguish the effects of climate plant use of fog N, or whether greater amounts of fog N in and canopy light effects on photosynthetic performance of foggier redwood forests are the reason for enhanced LUE. a particular species or plant community. Nonetheless, our Overall, our data demonstrate that plants growing under study species exhibited increasing A60 with decreasing lower light conditions show rapid induction once trans- light transmittance, consistent with other studies that char- ferred to high light, and that the ability to maintain sto- acterize the dependence of induction state on light habi- mata relatively open during diffuse light periods is asso- tat (Chazdon and Pearcy 1986a, b; Valladares et al. 1997; ciated with rapid attainment of maximum steady state Montgomery and Givnish 2008). Additionally, greater LUE photosynthesis when exposed to high light. The main at the wettest site is consistent with adaptations well suited difference among sites was the ability to continue photo- to enhance plant performance under low light conditions. synthetic activity immediately after a lightfleck, with four Thus, although the presence of fog reduces the amount of out of five species exhibiting increased photosynthetic sunshine, the associated moisture inputs also appear to pro- parameters associated with post-illumination CO2 fixation vide conditions that favor C gain during lightflecks, thus with increasing moisture. Greater foliar N with increas- buffering redwood understory plant species in northern ing moisture inputs in three species and the large sea- sites from extremely low C budgets. sonal change in leaf δ15N at the foggiest site suggest that Variation in foliar N concentration and δ15N among N inputs associated with fog also increase plant-available sites is also noteworthy. The increase in leaf N in three N that can be allocated to photosynthetic light-harvesting out of five species with increasing moisture inputs is in complexes and carboxylating enzymes to enhance C gain line with the idea that fog and rain contribute to plant N in low light (Evans 1989; Pasquini and Santiago 2012). uptake. However, the mechanism is unknown. One pos- Yet, further N isotopic work is clearly needed to nail down sibility is that greater fog and rain deposition in northern this hypothesis. These results highlight the potential for sites promote solubility of plant-available N forms in soil. variation in resource availability along environmental gra- Another possibility is that because rain, and especially dients to influence C gain opportunities for plants in low fog contain N (Weathers and Likens 1997; Weathers et al. light habitats.

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Acknowledgments We enthusiastically acknowledge Stefania Eller CB, Lima AL, Oliveira RS (2013) Foliar uptake of fog water and Mambelli and Paul Brooks for careful foliar N and isotope analyses; transport belowground alleviates drought effects in the cloud for- Vanessa Boukili, Anna Simonin, Art Fredeen and Rick Hatcher for est tree species, Drimys brasiliensis (Winteraceae). New Phytol faithful assistance in the field; Kevin Simonin, Kevin Tu, and Damon doi:10.1111/nph.12248 Bradbury for endlessly intriguing conversations on the complex eco- Engelbrecht BMJ, Herz HM (2001) Evaluation of different methods system processes in California redwood forests; Emily Burns (Limm) to estimate understorey light conditions in tropical forests. J Trop for taking an interest understory plants and providing key insights; Ecol 17:207–224 the California State Park System for access to sites; and the rangers Evans JR (1989) Photosynthesis and nitrogen relationships in leaves at Prairie Creek State Park for lively discussions over bonfires. The of C3 plants. Oecologia 78:9–19 University of California provided logistical support. Funding was Ewing H, Weathers KC, Templer PH, Dawson TE, Firestone MK, provided by a National Science Foundation Postdoctoral Fellowship Elliott AM, Boukili VKS (2009) Fog water and ecosystem func- (BIO-0310103) to L. S. S. and Mellon Foundation and Save the Red- tion: heterogeneity in a California redwood forest. Ecosystems woods League awards to T. E. 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