The contribution of fog to the water relations of Sequoia · PDF file ·...

Plant, Cell and Environment

(2004)

27

, 1023–1034

© 2004 Blackwell Publishing Ltd

1023

Blackwell Science, LtdOxford, UKPCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2004? 2004

27810231034Original Article

Contribution of fog to the water relations of coast redwoodS. S. O. Burgess & T. E. Dawson

Correspondence: S.S.O. Burgess, (present address) School of PlantBiology, University of Western Australia, 35 Stirling HighwayCrawley WA 6009 Australia. Fax: + 61 86488 1186; e-mail:[email protected]

The contribution of fog to the water relations of

Sequoia sempervirens

(D. Don): foliar uptake and prevention of dehydration

S. S. O. BURGESS & T. E. DAWSON

Department of Integrative Biology, University of California, Berkeley, CA 94720 USA

ABSTRACT

Fog is a defining feature of the coastal California redwoodforest and fog inputs via canopy drip in summer can con-stitute 30% or more of the total water input each year. Agreat deal of occult precipitation (fog and light rain) isretained in redwood canopies, which have some of the larg-est leaf area indices known (Westman & Whittaker,

Jour-nal of Ecology

63, 493–520, 1975). An investigation wascarried out to determine whether some fraction of inter-cepted fog water might be directly absorbed through leafsurfaces and if so, the importance of this to the water rela-tions physiology of coast redwood,


.An array of complimentary techniques were adopted todemonstrate that fog is absorbed directly by

S. sempervi-rens

foliage. Xylem sap transport reversed direction duringheavy fog, with instantaneous flow rates in the direction ofthe soil peaking at approximately 5–7% of maximum tran-spiration rate. Isotopic analyses showed that up to 6% of aleaf’s water content could be traced to a previous night’sfog deposition, but this amount varied considerablydepending on the age and water status of the leaves. Oldleaves, which appear most able to absorb fog water wereable to absorb distilled water when fully submersed at anaverage rate of 0.90 mmol m

2

s----

1

, or about 80% of transpi-ration rates measured at the leaf level in the field.

Sequoiasempervirens

has poor stomatal control in response to adrying atmosphere, with rates of water loss on very drynights up to 40% of midday summer values and rates above10% being extremely common. Owing to this profligatewater use behaviour of

S. sempervirens

, it appears that foghas a greater role in suppressing water loss from leaves, andthereby ameliorating daily water stress, than in providingsupplemental water to foliar tissues

per se

. Although directfoliar absorption from fog inputs represents only a smallfraction of the water used each day, fog’s in reducing tran-spiration and rehydrating leaf tissues during the most activegrowth periods in summer may allow for greater seasonal

carbon fixation and thus contribute to the very fast growthrates and great size of this species.

Key-words

: fog; water relations; redwood; sap flow.

INTRODUCTION

Fog as a meteorological phenomenon

Fog is a significant climatic contributor to a number ofterrestrial ecosystems (Weathers 1999). These includecoastal mountain regions where orographic lifting of moistocean air produces adiabatic cooling, condensation and fogformation. Sections of the Chilean and Peruvian Andes aregood examples of this and cloud forests such as in CostaRica are also included in this category. Low-lying coastalregions that are skirted by cold ocean currents experienceadvection fog, where warm ocean air crosses a band of coldwater before reaching land. Examples include Newfound-land (Labrador current), Namibia (Benguela current), andCalifornia (California current). Orographic and advectionfogs rely on wind to move air over a physical feature(mountain or band of cold water) which creates cooling;often both features are present, such as in the case of Chile.Because these fogs are wind driven, interaction with landsurfaces is greatly increased (see Oberlander 1956). A third,fairly ubiquitous type of fog occurs whenever radiative heatloss cools the Earth’s surface below the dew point of thesurrounding air. Such ‘ground fogs’ tend to form on stillnights and since a strong wind component is lacking, thereis less interaction with terrestrial surfaces.

The small (1–40

m

m, Prada & da Silva 2001) waterdroplets that comprise fog do not readily precipitate outof air unless they encounter the surface of solid objects(the vertical settling rate is too slow). As a consequence,fog rarely registers on a typical rain gauge and is there-fore termed occult (hidden) precipitation. Precipitation offog droplets mostly occurs by horizontal interception byterrestrial surfaces. Objects such as plant canopies, whichare fairly permeable to the through-flow of air and have alarge surface area, are ideal fog interceptors (e.g. seeKerfoot 1968).

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S. S. O. Burgess & T. E. Dawson

© 2004 Blackwell Publishing Ltd,

Plant, Cell and Environment,

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Fog as an ecological phenomenon

There are a number of potential outcomes when fog inter-acts with plant canopies. First, fog largely eliminates theatmospheric vapour pressure deficit that drives evaporationand transpiration from plant surfaces. Second, as winddrives a steady stream of fog droplets through the canopy,fog water builds up and wets leaf surfaces. Considerablewater can be held or ‘stored’ on canopy surfaces and if thiscapacity is not exceeded during fog deposition, this watersimply returns to the atmosphere with subsequent evapo-ration (Juvik & Nullet 1995). If water accrues on plantsurfaces beyond a certain storage capacity, water will dripfrom leaves onto soil or be funnelled to soil via stemflow(Hutley

et al

. 1997). At a study site in northern California,Dawson (1998) estimated that 34% of the annual hydrolog-ical input was via fog drip. Once fog drips onto soil, it canbe absorbed by the root systems of plants and Dawson(1998) demonstrated that a large fraction of water tran-spired by

S. sempervirens

and understorey plants in Cali-fornia’s fog zone originates from fog. A third possibility isthat the leaves of plants absorb water vapour directly froma saturated atmosphere (Breazeale, McGeorge & Brea-zeale 1950; Haines 1952, 1953) or from wetted leaf surfaces(Yates & Hutley 1995; Martin & von Willert 2000). Thereis substantial anecdotal evidence, and some experimentaldata largely from laboratory work (Kerfoot 1968), to sug-gest that leaves can absorb fog water by both processes,with greater absorption being possible from wetted surfacesthan directly from the atmosphere (Breazeale

et al

. 1950;Yates & Hutley 1995). For both processes, quantitative dataare generally lacking, particularly for plants growing in fieldconditions and, in addition, the pathways for foliar absorp-tion of water are poorly understood. In certain species (e.g.

Crassula

spp.), epidermal hydathodes (which are usuallyinvolved in guttation) play a role (Martin & von Willert2000). Hydathodes represent a gap in both the leaf cuticleand epidermis and their ability to exude water presumablycorrelates with their ability to absorb water. In the absenceof hydathodes, a cuticular pathway is usually presumed (e.g.Yates & Hutley 1995) and cuticular wettability, integrityand permeability vary considerably (Boyce, McCune &Berlyn 1991; Jagels 1991; Schreiber

et al

. 2001). The bark oftwigs has also been shown to absorb water (at least underpressure, Katz

et al

. 1989) but in this article we will focuson foliar uptake only.

An ecological role for foliar uptake of water has longbeen recognized (Rodin 1953; see Stone 1957 for review),particularly for arid habitats where other forms of precipi-tation are lacking (e.g. the Namib desert, Chilean high-lands). In places such as coastal California that do receiverainfall, the timing of fog events is important (Dawson1998). California’s Mediterranean-type climate is charac-terized by long summer droughts and it is during theseperiods that advection fogs are common. The role of fog inameliorating summer water deficits in coastal vegetation istherefore potentially large. This is particularly true for thecoast redwood


(D. Don) whose

native distribution today appears constrained to fog-inundated regions of the Californian and Oregon coastline.Although northern limits to the range of coast redwoodsare likely constrained by other factors (e.g. competition,cold temperature; Noss 2000), the southern and easternlimits appear tightly defined by areas subject to frequentand intense summer fogs (Cannon 1901; Cooper 1917).


is a shallow-rooted species and there-fore presumably does not benefit from access to stablegroundwater resources. Dawson (1998) has previouslydemonstrated that fog-drip onto soils is an important sup-plement to shallow soil water resources. Nevertheless,

S.sempervirens

is one of the tallest tree species and transport-ing limited soil water to leaves growing at heights well over100 m involves significant resistance due to friction andgravity. In this present study, our aim was to build on thisearlier work on inputs to soil water via fog drip and inves-tigate other potential contributions of fog to the plant’swater relations: conservation of plant water resources bysuppression of transpiration and direct foliar absorption offog water as an alternative pathway of plant hydration. Weemployed a number of complimentary methods and usedboth field observations and controlled-environment exper-iments to explore the importance of fog to the water rela-tions of the world’s tallest tree species.

MATERIALS AND METHODS

Field site description

The study site consisted of a small (11 ha) patch of oldgrowth redwood forest growing on a flat ridge (300 m alti-tude) in Sonoma County, CA (38

∞

24

¢

N, 122

∞

59

¢

W) approx-imately 8 km from the ocean. Satellite photographssuggested the site was subject to frequent fog inundation(http://www.nrlmry.navy.mil/sat-bin/lowcloud.cgi). The landbetween the forest and the ocean is largely under viticul-ture and the lack of physical barriers allows fog to moveunimpeded inland to the site.

Two groups of three trees were selected for study, one ofthe extreme west (seaward) edge of the forest stand andone approximately 200 m east within the forest stand. Thegroups of three trees were selected such that the trees wereof a similar height (60–70 m) and girth (approximately1.5 m diameter) and grew within a 12 m radius (owing tothe logistics of equipment deployment). Preliminary data(Roden, Johnstone and Dawson, unpublished) indicate thatthe trees were approximately 350 years old. At each groupof three trees, climbing ropes were installed to facilitatecanopy access.

Field observations

Sap flow

We opted to use the heat ratio method (HRM: Burgess

et al

. 2001a, b) to measure sap flow in

S. sempervirens

spec-imens because of its ability to measure the slow rates offlow expected during foggy conditions that result in low

http://www.nrlmry.navy.mil/sat-bin/lowcloud.cgi

Contribution of fog to the water relations of coast redwood

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vapour pressure deficits. The HRM’s ability to measurereverse flows (Burgess, Adams & Bleby 2000) was also key,as we hypothesized that foliar deposition and potentialuptake of fog water could result in transport of waterthrough the xylem in the opposite direction to that due totranspiration.

Probe construction

Thermocouple temperature probes were constructed byplacing two insulated fine gauge (36 AWG) copper–constantan thermocouple junctions inside a stainless steelhypodermic needle (18 gauge/1.3 mm diameter and38 mm in length). The thermocouple junctions werespaced such that their final positions within the stainlesssteel needle were 5 and 20 mm from the needle tip. Theneedle tip was sealed with solder and the needle basefilled with epoxy resin to secure and waterproof the con-tents of the probe.

Line heater elements were formed by tightly coiling a 15-cm length of nichrome wire (36 AWG, 95

W

m

-

1

) and insert-ing the coil into a 10-

m

L glass capillary before placing it ina 38-mm long needle.

Probe installation

For each group of three trees at each site, 16 sap flowsensors, each capable of measuring sap velocity at tworadial depths (15 mm apart) were installed. Eight sen-sors were installed at breast height in the stems of thethree trees and spaced approximately 120

∞

around thecircumference of each tree (only two sensors were avail-able for the third tree). Due to the thick bark of

S. sem-pervirens

(up to 15 cm for our trees), an 8-cm diameterhole-saw, followed by hand chisels, was used to removebark until just before the living cambium (light pinkcolour). A steel drill guide was built into a frame thatallowed the drill guide to be inserted and secured flushon the stem within the 8-cm hole. A drill was equippedwith a long-shank chuck small enough to pass within theframe and drill the three 1.35 mm diameter, 40 mm-deepholes required for probe installation. Otherwise probeinstallation was the same as described by Burgess

et al

.(2001a).

System wiring

The probes were connected by 6 m-long cables to a cen-trally placed AM416 multiplexer (Campbell Scientific Inc.,Logan, UT, USA), with thermocouple circuits differentiallywired to minimize electrical noise and with heater probecircuits connected to a distribution strip mounted in themultiplexer enclosure. A temperature thermistor wasplaced on the multiplexer to serve as a reference for ther-mocouple measurements. Two shielded four-conductorcables were used to connect the multiplexer to a datalogger(CR10X, 2MB extended memory; Campbell Scientific Inc.)mounted 25–30 m above the multiplexer in one of the trees.

Multiplexer control and data transmission circuits wererouted to separate four-conductor cables to avoid electricalinterference.

An additional eight sensors were deployed at between 50and 55 m height in the upper canopy of one the three trees.Two sensors were placed in the stem and the remaining sixplaced in three branches. For each branch, one sensor wasplaced on the top and one on the underside of the branch.Selected branches were generally 0.1–0.2 m in diameter andfaced different aspects. The stem at this height was usuallyapproximately 0.5 m diameter. Due to the thinner bark instems and branches at this height within the tree, the above-mentioned tools and techniques were not required to installprobes.

Once again the eight sensors were multiplexed via anAM416 and connected to the datalogger 25–30 m belowusing two four-conductor cables. A third, two-conductorcable was used to connect a 30-W solar panel to thedatalogger’s battery (40 A h sealed gel-electrolyte type).During measurements, the solar panel was disconnectedfrom the battery using a relay so as to avoid electricalinterference. A 30-m nine-pin serial cable was alsoattached to the datalogger so that data could be collectedfrom ground level. The central placement of the datalog-ger in this two-multiplexer, 16-sensor system minimizedcable lengths for data transmission and therefore theeffects of electrical noise. Power supply for the heaterprobes was switched using a relay placed in the datalog-ger enclosure. Voltage drop was substantial with this wir-ing scheme, but heaters still provided up to 1

∞

C heating.Further increases to heater circuit resistance (e.g. longercable-lengths) would warrant power supplies closer to theheaters.

At the end of the data collection period, a subset of thesap flow data was validated by drilling a series of holes toform a 5–6 cm-wide slice immediately above the site ofprobe installations. This was done to stop sap flow near thesites of probe installation without damaging the treesexcessively. In this way, a reference velocity (zero) couldbe imposed to calculate the zero offset value of the probeand allow data to be corrected according to the proceduresoutlined by Burgess

et al

. (2001a). This approach permitsthe most accurate discrimination between water loss (indi-cated by xylem sap flow in the direction of leaves) anduptake (reverse flow). To prevent damage to the studytrees and allow other sensors to continue operating, datafrom only a few representative sensors were validated andthe data corrected this way. Based on the results fromthese examples, environmental conditions were estab-lished which allowed us to estimate when flow rates werezero in the remaining sensors. The conditions were: humid(

>

94%) and still pre-dawn periods (0300–0600 h) whenleaves were not wet. At the potential cost of reduced accu-racy, this indirect method allowed us to interpret data fromprobes that were not cut. Figure 2 includes two probes thatwere corrected by interrupting flow to establish zero flowand a third sensor (stem at 1 m) corrected using the abovecriteria.

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Meteorological data

In each group of three trees, the following meteorologicalmeasurements were made at the same height (50 m) wheresap flow was measured in branches and the upper stem.

1

An index of within-canopy photosynthetically activeradiation and total radiation, using a pyranometer andquantum sensor (LI-COR Inc., Lincoln NE, USA)placed on a horizontal branch.

2

Temperature and relative humidity (Model CS500;Campbell Scientific Inc.).

3

Leaf wetness, using three wetness-sensing grids (Model237; Campbell Scientific Inc.) placed horizontally 2 mfrom the stem on three branches facing different aspects.Leaf wetness sensors measure resistance of a gold-platedsensing grid in k

W

. When completely dry, the sensor readsas an open circuit and a mostly dry circuit reads in thehigh thousands (k

W

). A very wet circuit (i.e. with visibledeposition of water) reads approximately 0–10 k

W

. Thegeneral response of the sensor is logarithmic and so datahave been log-transformed (see Fig. 1) and then multi-plied by 10 to give a crude index of leaf wetness wherezero is completely saturated and 10 or above is dry.

These measurements were recorded by a datalogger placedat 50 m within the canopy but controlled from ground levelvia a 60 m, nine-pin serial cable (at 1200 baud to accommo-date the longer cable length).

Fog collector

A fog collector was constructed after the design of Juvik &Nullet (1995) and installed at 50 m height in a tree crownat the forest edge. The collector was constructed of a cylin-der of louvered aluminium screen measuring 17.8 cm indiameter and 60 cm in height. This cylinder was mountedonto a standard tipping bucket rain gauge (RainWise Inc.Bar Harbor, ME, USA) that was connected to a datalogger.A circular rain shield measuring 60 cm in diameter wasmounted on the top of the fog collector to prevent verticalprecipitation (rain) from entering the collector. Rain drivenby strong winds is probably problematic for this instrumentand for this reason a standard rain collector makes a usefuladjunct so that rain events can be recognized and dis-

counted. During the course of this experiment, the fog col-lector underwent development due to unreliablemeasurements in the early part of the experiment. As aconsequence, we did not obtain continuous data recordsfrom the fog collector during the study period. Instead, toconstruct long-term fog records for the study period weused leaf wetness sensors and rain gauges as a proxy. When-ever leaves were wet for more than 3 h in the absence of arain event, fog was presumed as the cause. This method wascompared with, and agreed well with the portions of extantdata from the fog collector (see Fig. 1). Dew events cannotbe separated from fog using this method, but for the pur-poses of this investigation this is not important since thephysiological effects of dew (see Boucher, Munson & Bern-ier 1995) are probably similar to those of fog.

Glasshouse experiments

Two, 2-m-tall potted redwood saplings were placed in aclear polyvinyl chloride (PVC) ‘fog’ chamber(2 m

¥

1.2 m

¥

1.2 m) inside a glasshouse. A single HRMsensor containing two pairs of thermocouples was placed inthe base of the sapling’s stem (50 mm diameter). Two fur-ther, miniaturized HRM sensors (see Burgess, Dubinsky &Dawson 2001 for more details) were installed on two dif-ferent 6-mm-diameter branches. Readings were madeevery 10 min and averaged hourly. As absolute flow rateswere not required to investigate the importance of wateruptake by leaves relative to transpiration rates, sap flowdata are expressed as a percentage of maximum rates mea-sured for each sensor during the experiment. Although theexperiment was carried out during winter, the maximumrates of flow measured on warm, sunny winter days in theglasshouse were probably not much lower than true maxi-mum values. Zero-offset values and appropriate correc-tions for all sensors were obtained by taking night valueswhen the PVC chamber was fully closed to prevent waterloss.

An ultrasonic device (Chaoneng Electronics, Nanhai,Guangdong, China) was placed in a reservoir of distilledwater maintained at a given capacity by means of a floatswitch and used to generate fog at a rate of 500 mL h

-

1

. Thisdevice was chosen to produce a water aerosol that resem-

Figure 1.

A comparison of the perfor-mance of leaf wetness sensors, humidity sensor and fog collector during fog and non-fog conditions. Relative humidity (plain line) is plotted on the left axis and leaf wet-ness (line with circles) is plotted on the right axis in k

W

of resistance (values less than 10 indicate liquid water deposition to leaves). Fog deposition measured by the fog collec-tor is plotted on the left axis. For the sake of scale, units are grams of water collected per m

2

of collecting surface area every 30 min.


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bled ‘typical’ fog as closely as possible, namely with drop-lets in the 1–40

m

m range, as opposed to sprayingtechniques which have more similarity with light rain. Sincethe artificial fog rapidly coated leaf surfaces with a film ofliquid water, droplet size was probably a less importantdistinction than the evenness with which an aerosol cancoat surfaces. A small electric fan was used to disperse thefog and circulate it throughout the chamber. By means ofan electronic timer, fog events of various durations couldbe applied to the tree. After each fog event, the sides androof of the PVC chamber were removed to ventilate theplant and allow leaves to dry off. Prior to initiation of anyfog event, extreme care was taken to double or triple bagthe pot and root system of the sapling to prevent any fogwater from reaching the soil by any means other than xylemtransport (i.e. including stem flow).

Isotope experiments

As described for the above glasshouse experiment, 2-m-tallsaplings were placed in the ‘fog chamber’. A ‘labelled’ watersource with a hydrogen isotopic composition (

d

D

) of +6‰,was added to the reservoir that supplied the ultrasonic foggenerator. We measured the isotopic composition of theresultant fog and it did not differ from the water in thereservoir (data not shown) because ultrasound atomizes,rather than evaporates water.

The isotopic composition of tap water used to irrigate thesaplings had a

d

D

of

-

78‰. All isotopic values wereexpressed in standard delta notation (parts per thousand,or ‰) relative to the V-SMOW (Vienna Standard MeanOcean Water) standard:

A simple proportional mixing model (as reviewed by Daw-son

et al

. 2002) was used to determine the proportion ofwater in leaves that was derived from fog water versusirrigation water.

Two treatments were considered: water-stressed plantsversus well-watered plants and young leaves versus oldleaves. Well-watered plants were irrigated such that leafwater potentials were maintained at approximately

-

0.5 MPa. Irrigation was withheld from plants in the ‘water-stressed’ treatment until leaf water potentials reached

-

1.65 MPa.Saplings were fogged overnight using the same methods

described above and then removed from the PVC chamberfor sampling. Droplets of water shaken from branches werecollected to verify that deposited fog water retained the 6‰isotopic label. For each treatment, nine leaf samples (threeleaves each from three different saplings) were collected.Leaves were quickly but thoroughly dried with paper toweluntil no water remained on leaf surfaces. Additional leafsamples were also dried and used to measure leaf waterpotential. Water was extracted from sample leaves by cryo-genic vacuum distillation (Ehleringer, Roden & Dawson2000). The isotope ratio of each water sample was deter-

dD = -ÈÎÍ

˘˚̇

¥2 1

2 1 1 1000H HH H

Standard

Sample

//

mined by combusting approximately 2

m

L of water in thepresence of hot (800

∞

C) Cr using the H/Device interfaceattached to a Finnigan MAT delta-plusXL isotope ratiomass spectrometer (Bremen, Germany).

Laboratory experiments

In order to measure the rate at which a

s. sempervirens

leafcan absorb water when its surface is completely wet, thefollowing experimental apparatus was devised: an elec-tronic balance (Denver Instrument, Denver, CO, USA; res-olution 0.01 mg) was attached to a computer to allowweight changes to be recorded every 30 s. A 50-mL vial wasplaced on the balance and filled with deionized water. Foreach experiment, a single leaf-bearing branchlet, represent-ing 1 year’s growth, from a potted redwood sapling wasimmersed in the vial and the supporting branch held firmlyin place by a retort stand clamp. A layer of vegetable oilapproximately 3 mm thick was added to the water in thevial to prevent evaporation. The sapling and balance wereplaced in a dark room and left without disturbance forapproximately 3 d. At the end of each experiment, the por-tion of branchlet and leaves immersed in water was excisedand the leaf area was measured with a leaf area meter (LI-3000: LI-COR Inc.).

As an adjunct to our absorption experiments, we alsoexamined the surfaces of a number of

S. sempervirens

leaves using scanning electron microscopy (Electroscan E3ESEM; Wilmington, MA, USA).

RESULTS

Field experiments

Sap flow

Figure 2 shows sap flow and meteorological conditionsover a four day period at the end of the summer fog sea-son (mid-May to late October) in early October 2001,when no significant rain had been recorded for 3 months.Data from this period are representative of similar sapflow patterns associated with heavy fog on over 20 occa-sions during the rainless ‘fog season’ in 2001 and in thesubsequent 2002 and 2003 fog seasons. The sap flow pat-terns displayed in Fig. 2 agreed with patterns in all othertrees measured during this period. Figure 2a shows xylemsap flow measured by a single sensor placed in the lowerstem (1 m), upper stem (50 m height) and lateral branch(50 m height) of a redwood at the edge of the forest sitein Sonoma County. For the purposes of comparison inFig. 2, the differing flow rates found in the different partsof the tree measured were ignored and values were nor-malized with respect to maximum values for each sensorfor this time of year. This permits a clear comparison ofthe timing and relative proportions of positive andreverse sap flow at each measurement position within thetree.

Figure 2b demonstrates a range of meteorological con-ditions over the 4 d period presented, including two fog

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events of different magnitude. When compared withFig. 2a, a number of important aspects of redwood phys-iology and water relations are revealed. The first nighthad low relative humidity (approximately 20–40%),resulting in night-time water loss from the canopy (seealso Fig. 3). Meteorological conditions on day 1 pro-duced a typical pattern of daytime transpiration,although maximum rates under October conditions ofsolar insolation were approximately 70% of mid-summerrates. Night 2 indicates heavy fog conditions. Relativehumidity was 100% and in addition, leaf wetness sensorsindicated near-saturation. During this period the fog col-lector logger was damaged, so fog was inferred by thecombination of high humidity, wet leaves and absence ofrain as measured in an adjacent vineyard. Sap flow dur-ing night 2 was near zero or very slightly negative. Onday 2, heavy fog persisted, resulting in a completeabsence of transpiration. Instead, rates of reverse flowincreased at all positions within the tree; maximumreverse flow rates measured were approximately 5–7%of maximum transpiration rates. By approximately1600 h, the leaf wetness sensors showed some evidenceof drying, however, this was incomplete and relativehumidity remained extremely high. Relative humidityremained above 90% for the duration of night 3; sapflow was approximately zero during this time. Sap flow

rates were fairly normal on day 3, with humidity levelsbeing low enough to permit some transpiration (relativehumidity = 75%, vapour pressure deficit = 0.4 kPa).Humidity was once again very high on night 4 (rangingfrom 90 to 97%), however, the absence of readings bythe leaf wetness sensor suggests there was no fog orfog-deposition on this night. Note that by dawn, sapflow rates were zero in all parts of the tree. Day 4 wassimilar to day 3. Finally, on night 5, fog returned, asindicated by relative humility values of 100% and leafwetness sensors indicating deposition of water; againreverse flow was detected.

A strong relationship between night-time (0030–0530 h)sap flow and vapour pressure deficit was evident for

S.sempervirens

(Fig. 3). Expressed as percentage of maxi-mum flow rate measured in the study tree, night-timerates of water loss often exceeded 20% of peak water lossrates measured at noon under hot summer conditions. Onone or two extremely dry nights, water loss rates exceed-ing 40% of maximum were recorded (see Fig. 3); smallervalues of 10–12% such as in Fig. 2a are very common.The possibility of very large rates of night-time water lossas indicated in Fig. 3 is supported by data from the 24other extant sets of measurements at the study site: peakrates of night-time water loss averaged 37% of summermaximum.

Figure 2.

(a) Four days of sap flow data at the three different positions in a single


tree. To facilitate com-parison among the different flow magni-tudes in different parts of the tree, data are normalized by expressing flow rates as a per-centage of summer maximum values for each sensor. This also allows comparison of maximum rates of water uptake with maxi-mum rates of water loss. (b) Relative humid-ity (thin line) is plotted on the left axis and leaf wetness (line with circles) is plotted on the right axis in k

W

of resistance. Laboratory calibrations demonstrate that values less than 10 indicate liquid water deposition to leaves. Values greater than 10 indicate a moist atmosphere but without the build-up of a water film. Missing values indicate an ‘open circuit’ or completely dry sensor.

(a)

(b)


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Meteorological measurements

Figure 4a shows the number of days and nights with rainfallevents for each month during the sampling period.Figure 4b shows the number of days and nights with fogevents. Figure 4c shows monthly totals of heat pulse veloc-ity (a simple proxy for sap flow; see Burgess

et al

. 2001a)averaged for trees at both the edge and interior sites withinthe forest. Evapotranspiration measured by the City ofSanta Rosa approximately 40 km inland from our coastalsite (beyond the typical reach of fog) is also plotted next tothe rainfall and fog data for each period. Comparing thesedata with each other at each single time period and alsoacross the entire year, we note that monthly sap flow totalsgenerally tracked closely the measurements of evapotrans-piration inland from our site. However, large discrepanciesappear particularly during August when fog was heaviest.

Glasshouse experiments

Figure 5 shows xylem sap flow rates (expressed as percent-age of maximum) in the stem and a single branch of a 2-m-tall redwood sapling over a 5 d period. At approximately1100 h on day 3, a 10 h fog event was initiated. For context,we calculated that water uptake by the two 6 mm branches(averaged in Fig. 3) of the 10 h fog period totalled 18% ofwater lost by these branches on day 5. In the main stem,water uptake totalled 6% of water loss of day 5. This value

was decreased in part by the brief period of water loss inthe early stages of the fog event when fog had not built upsufficiently to cover the top of the sapling. Apparently atthis point, water was still being lost by upper branches whilelower branches with wet leaves were absorbing water.Although sap flow reversals in response to fogging wereeasily repeatable, we could not detect any repeatableincreases in soil moisture in response to foliar uptake of fogwater using capacitance sensors (CS615; Campbell Scien-tific Inc., data not shown).

Isotope experiments

Based on a simple mixing model, the proportion of leafwater sourced from fog water was 6.4% in old leaves fromwell-watered plants (Fig. 6). In contrast, young leaves fromwell-watered plants only contained 1.8% fog water. Forwater-stressed plants, values were 1.6% for old leaves and1.2% for young leaves.

Laboratory experiments

When placed in distilled water, leaf-bearing branchlets (1–3 years old,

n

= 3) absorbed water fastest during ‘usual’daylight hours (the plant remained in continuous dark) andhardly at all during hours of usual darkness (Fig. 7). Theaverage rate of absorption, approximately 0.89 mmol m

2

s

-

1

, was about 80% of typical leaf-level transpiration valuesmeasured (

n

= 58) in the field during August using a porta-ble photosynthesis measurement system (LI-6400; LI-CORInc.). Note that the weight changes shown in Fig. 7 repre-sent export of water from the portion of leaf submersed inthe vial into the rest of the plant: localized absorption ofwater into leaf tissue would increase the leaf’s volume anddisplacement resulting in no net change in the weight of thevial.

Microscopy

Despite the mesic habitat of

S. sempervirens

, leaves had athick cuticle, stomata were recessed and each stomatal porewas capped by an epicuticular wax plug. Non-pathogenicfungal hyphae were often observed entering stomatal pores(Fig. 8) and this appeared to be more common on matureleaves where the epicuticular wax plug was degraded.

DISCUSSION

The prolonged and heavy fog event documented in Fig. 2yields one of the clearest examples of sap flow reversal thatindicates direct foliar uptake of water by a large

Sequoiasempervirens

specimen under field conditions. Whilenumerous, brief fog events were accompanied by indica-tions of sap flow reversal in all of the trees we measured,the largest magnitude and therefore most definitive flowreversals were seen when fog events were heavy for a wholedaylight period (as shown in Fig. 2). Sap flow reversals dur-ing fog events were always small in magnitude (sap veloci-

Figure 3.

Relationship between night time sap flow and vapour pressure deficit (kPa) in


derived from 1361 measurements made between midnight and 0600 h during spring and summer 2001 in the edge tree at Sonoma. (Note that the line of best fit ignores negative values associated with water uptake). Sap flow rates are expressed as a percentage of maximum transpi-ration rate observed for this sensor during summer. Night-time flow rates in response to vapour pressure deficit often exceeded 20% of maximum summer transpiration and on one or two occa-sions rates of over 40% were recorded.

Xyl

em s

ap fl

ow (

% o

f max

imum

)

1030




27,

1023–1034

Figure 4.

(a) Number of days and nights with rain for a year-long period of obser-vations at the Sonoma site. (b) Number of days and nights for the same period hav-ing fog events sufficient to cause leaves to become wet for at least 3 h. Note that the data presented in Fig. 4a and b are mutu-ally exclusive because we have defined fog as strictly an occult precipitation event: any rain measurements preclude designa-tion as fog. (c) Monthly sap flow totals (m month

-

1

, using heat pulse velocity as a proxy) for


, aver-aged for all measurement positions (Edge and Interior) at Sonoma study site and evapotranspiration (ET, mm) measured by the City of Santa Rosa approximately 40 km inland from our study site.

Figure 5.

Sap flow rates in the stem (aver-age of measurements at two positions) and branches (average of measurements in two 6 mm diameter branches) of a 2-m-tall potted


sapling growing under glasshouse conditions. Fog was applied at approximately 1100 h on day 3 and main-tained for 10 h.


1031

© 2004 Blackwell Publishing Ltd, Plant, Cell and Environment, 27, 1023–1034

ties 1–1.5 cm h-1), often approaching the limits of accuracyof the HRM (approximately 0.5 cm h-1) and thus we areonly confident to discuss sap flow reversals for the largestexamples. Furthermore, the data we present in Fig. 2 wererecorded just days before the xylem surrounding the probeswas interrupted by cutting to establish a true zero value.The possibility for any drift in the zero line for these setsof measurements was therefore minimized. By means ofthese prompt validations we obtained very fundamentalevidence that flow reversals did indeed increase the ratioof heat flux in the direction of the soil versus the leaves, ascompared with baseline heat ratios measured when xylemwas severed a few days later. The fact that flow reversalswere measured simultaneously throughout all parts of thetree adds strength to our interpretation of the sap flow dataand further suggests a whole-plant, leaf–soil flux wasinvolved. Laboratory data such as those of Slayter (1956)which showed whole-plant reverse water transport throughPinus echinata seedlings in response to a vapour pressuregradient create something of a precedent for our observa-tions. Unlike Slayter’s (1956) laboratory experiment, wewere not in a position to gauge the amounts of water deliv-ered to roots and/or the soil/rhizosphere from our measure-

ments in the stem, but for reverse flows to move past ourlowest measurement position (1 m), one would expectincreases in the moisture content of root tissue at the veryleast. As an aside, it is interesting to note that duringreverse flow, the water potential gradient in the tree will beless than the hydrostatic gradient due to gravity. Gravitydictates that the minimum tension in the xylem at the topof a 60-m tree is approximately 0.6 MPa, but during reverseflow this value is clearly reduced.

The results from the glasshouse experiments agree wellwith the above conclusions drawn from our field-basedmeasurements. Flow reversals were of similar magnitude tothose measured in the field, although because the glass-house experiments were conducted in winter, flow reversalswere probably slightly overestimated relative to true max-imum transpiration rates. The fact that we could not detectincreases in soil moisture with capacitance sensors is puz-zling in view of the measured reversals in sap flow, however,the sensitivity and positioning of these sensors may nothave been optimal to detect such changes.

While attempting to measure sap flow reversals in thesaplings, we made unconfirmed observations that sug-gested that the longer the water was withheld from the

Figure 6. Proportion of water inside Sequoia sempervirens leaf tissues derived from foliar uptake of isotopically labelled fog water versus absorption of soil water at high (-0.5 MPa) and low (-1.65 MPa) leaf water potentials.

Figure 7. Water uptake by Sequoia sem-pervirens branchlets. Data are an average of three branchlets, each bearing approxi-mately 20 leaves (average projected leaf area =8.66 cm2). A strong diurnal rhythm was generally evident (note error bars) in rates of uptake, with peak rates reaching 2 mmol m2 s-1 (or 0.1 g h-1 for the whole leaf). The average rate of uptake was 0.9 mmol m2 s-1.

–

–

1032 S. S. O. Burgess & T. E. Dawson


plants, the harder it was to induce reverse flow by fog-ging. Although we did not set up an experiment to testthis, the results of our isotope labelling experiment sup-port these observations and indicate that, at least for oldleaves, water-stress reduces the capacity for foliarabsorption of water. This agrees with the findings of Vaa-dia & Waisel (1963), who showed that water stressreduced rates of foliar uptake in Pinus halepensis . Thelabelling experiments also suggest that if leaves are wellwatered, old leaves are more conducive to water uptakethan young leaves; this was also our (undocumented)experience with the submerged leaf experiments (seebelow). The various factors and conditions that mayenhance or reduce foliar uptake of water are worthycandidates for further, controlled experimentation. Inparticular, the role of fungal hyphae in altering the prop-erties of leaf surfaces warrants exploration. As leaf sur-faces degrade with age and are invaded by fungalendophytes, hyphae may form a ‘wick’ to move waterpast epicuticular waxes.

Magnitude and ecological significance of foliar uptake

Based on an allometric relationship supplied by Stancioiuand O’Hara (unpublished results), the tree from which thedata presented in Fig. 2a were collected had a projected leafarea of 660 m2. The laboratory-based water uptake experi-

ments using submerged leaves yielded an average absorp-tion rate of 0.058 L h-1 m-2 projected leaf area, or theequivalent of 38 L h-1 for the whole tree. Assuming a crudeestimate of rooting area of 80 m2 for each tree at our site,then over a 12-h period (e.g. midnight to noon) of foliarabsorption each tree would capture an amount of waterequivalent to a 5–6 mm rain event being fully absorbed bythe root-zone. Sap flow measurements did not suggestuptake anywhere near this magnitude, with a maximum rateof only about 1.5 L h-1 of water moving downward throughthe stem at breast height (0.225 mm rain equivalent over12 h). We see three likely reasons for this discrepancy. First,fully submersing leaves in distilled water for a prolongedperiod of time probably establishes conditions for waterabsorption that are quite different to those experienced inthe field. Second, the isotope experiments demonstrate hugevariability in rates of uptake depending on leaf age andphysiological condition (e.g. leaf water potential): the resultsfrom one type of leaf thus cannot be scaled to a wholecanopy comprised of a range of leaf types. These two reasonsprobably render our laboratory measurements of foliaruptake a gross overestimation from a whole plant perspec-tive. A third reason for the discrepancy is instead a potentialcause for underestimation of foliar uptake as measured bysap flow: much of water that is absorbed through leavesprobably first refills storage capacity in leaves, twigs andstem, allowing only a smaller remainder of fog water tomove past sap flow sensors toward roots and soil.

Figure 8. An electron micrograph of the surface of a Sequoia sempervirens leaf show-ing hyphae from an unidentified leaf fungal endophyte entering a single stoma (Courtesy A. Fábre).

Contribution of fog to the water relations of coast redwood 1033


Results of the submerged leaf experiments comparedquite poorly with our sap flow and isotopic studies. Becausethe latter two studies involved deposition of fog dropletsonto leaves rather full submersion of leaves into water, weare inclined to consider results of these experiments asmore realistic indicators of the potential of foliar uptake ofwater. This position is further strengthened by the fact thatthe sap flow and isotope experiments agreed quite wellwith one another. The fact that these experiments indicatethat foliar absorption of water is small in comparison totranspiration losses does not mean that fog is insignificantto the water budget of redwood trees. First, Dawson (1998)demonstrated a large role for unabsorbed fog water drip-ping onto soil where it can be accessed by roots. Second,fog dramatically suppresses transpiration by eliminatingatmospheric vapour pressure deficit (Byers 1953). Indeed,even if the flow reversals shown on day 2 in Fig. 2a wereignored, the water savings from a lack of positive flow(transpiration loss) are large compared to water losses ofadjacent days. From a water budget perspective, every fogevent like this shortens the drought period by 1 d, while atthe same time augmenting available water in the soil viafog drip and in the plant via foliar uptake. This may haveimportant consequences for daily and seasonal carbon fix-ation for S. sempervirens , which is one of the fastest grow-ing conifer species known (Noss 2000). The fact that, inproportional terms, monthly sap flow totals (Fig. 4c) werereduced compared to inland evapotranspiration duringAugust, which was the heaviest fog period (Fig. 4b), clearlydemonstrates that coastal fog attenuates transpiration dur-ing what would otherwise be a hot dry time of the year. Inother words, the coast-hugging S. sempervirens experiencesa much milder Mediterranean-type drought than it wouldinland.

Given the strong relationship between vapour pressuredeficit and night-time water loss (Fig. 3, see also Benyon1999) it appears that S. sempervirens has either poor sto-matal control in response to changes in vapour pressuredeficit, or incomplete stomatal closure (due to asymmetricguard cells resulting from polyploidy, Noss 2000). We rou-tinely measured night-time water loss rates up to 20% ofthe most rapid summertime transpiration rates. Given thelarge proportion of time S. sempervirens spends in the dark,significant amounts of water loss are possible during a timewhen there is no benefit of carbon gain. Figure 4b showsthat nearly one-third of the nights as opposed to only one-fifth of the days during August had heavy fog. Preventionof the rather disadvantageous loss of water during night isprobably just as important as attenuating daytime transpi-ration rates in dictating the observed distribution of S. sem-pervirens along fog-inundated coastlines.

As fog is most frequent at night, there are still plenty ofdays during the summer growing season when solar radia-tion is high and leaf surfaces are dry to permit maximumgas exchange and photosynthesis. It is likely that the avoid-ance of desiccation, coupled with supplements to stem, leafand soil water storage via foliar uptake and fog-drip wouldgreatly enhance leaf water potential (Menges 1994; Yates

& Hutley 1995), CO2 fixation and growth rate during theseconditions.

CONCLUSIONS

In addition to previously demonstrated hydrologic inputsvia interception and the dripping of fog water from cano-pies to the soil (Dawson 1998), we have demonstrated thatS. sempervirens can absorb small quantities of fog-waterdirectly through their leaves. The small amounts of foliaruptake are difficult to quantify, so we employed severalcomplimentary methods to build what we believe is a cau-tious estimate of fog uptake by leaves under conditionswhen it is maximal. Although amounts are small, they aresufficient to initiate reverse water flux throughout largetrees and improve the water status of the entire plant, pre-sumably including the root-zone. An impact sufficient to beseen at the whole plant level suggests that foliar uptakecould contribute meaningfully to recharge of water storeswithin plants, repair of cavitated conduits (Tognetti et al .2001), drive cell expansion and even lead to increased car-bon fixation. In addition, the potential for nutrient fluxesinto leaves from particulates deposited on leaf surfaces ordissolved in the fog itself (Azevedo & Morgan 1974; Weath-ers 1999; Weathers et al . 2000) is raised and warrants fur-ther study. Although the wax-plugged leaf surfaces of S.sempervirens do not appear to be efficient at absorbingwater (e.g. Feild et al . 1998 state that wax plugs preventwater films from forming on leaf surfaces), this may changeas leaf surfaces degrade with age and are invaded byhyphae from fungal endophytes (Fig. 8; see Rollinger &Langenheim 1993). Furthermore, in common with the wax-plugged leaves of Drimys granadensis (Feild & Holbrook2000), S. sempervirens are demonstrably inefficient at pre-venting water loss and it is in mitigating this that we believefog plays the most important role in this species that todayis restricted to the coastal fog-belt of California.

ACKNOWLEDGMENTS

Funding for this work was provided by the Andrew W.Mellon foundation and Global Forest (GF-18-2000-112/113). Many thanks go to Caryl & Mickey Hart and theSonoma Co. LandPaths organization for site access andassistance, Walt Chavoor & Theo Chavas (Kendall JacksonWinery) who provided rainfall data, the City of Santa Rosafor evapotranspiration data, Chet Moritz and Danika Gil-bert for risking their necks rigging the trees, Eric Dubinskyand Jia Hu for their dedicated hard work on all aspects ofthis project and also Primrose Boynton, Adeline Fabré,Ken Peer, Vanessa Schmitt and Spencer Hawkins for all oftheir assistance. We thank John Rumbold for helpful com-ments on the manuscript.

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Received 13 January 2004; received in revised form 6 April 2004;accepted for publication 13 April 2004

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