REVIEW
New Phytol.(2000), 147, 105-115
Researchreview
Responses of tree finerootsto temperature
KURT S. PREGITZER*, JOHN S. KING, ANDREW J. BURTON
AND SHANNON E. BROWN
School ofForestryand Wood Products,Michigan TechnologicalUniversity,
1400 TownsendDrive, Houghton,MI 49931, USA
Received12 November1999; accepted13 March 2000
SUMMARY
Soil temperaturecan influencethefunctioning
ofrootsin manyways. If soil moistureand nutrientavailabilityare
adequate, ratesof rootlengthextensionand rootmortalityincreasewithincreasingsoil temperature,at least up
to an optimaltemperatureforrootgrowth,whichseems to varyamong taxa. Root growthand rootmortalityare
in thefall.At present
mortality
highlyseasonal in perennialplants,witha flushofgrowthin springand significant
we do not understandwhetherrootgrowthphenologyrespondsto the same temperaturecues thatare knownto
controlshoot growth.We also do not understandwhetherthe flushof rootgrowthin the springdepends on the
utilizationof stored nonstructuralcarbohydrates,or if it is fueled by currentphotosynthate.Root respiration
increasesexponentiallywithtemperature,
but Qlo values rangewidelyfromc. 1.5 to > 3.0. Significantquestions
yet to be resolved are: whetherrates of root respirationacclimateto soil temperature,and what mechanisms
controlacclimationifit occurs. Limited data suggestthatfinerootsdepend heavilyon the importof new carbon
(C) fromthe canopyduringthe growingseason. We hypothesizethatrootgrowthand rootrespirationare tightly
linked to whole-canopy assimilation through complex source-sink relationships within the plant. Our
understandingof how the whole plant respondsto dynamicchanges in soil temperature,moistureand nutrient
resourceschange simultaneously
availabilityis poor, even thoughit is well knownthatmultiplegrowth-limiting
throughtime duringa typicalgrowingseason. We reviewthe interactionsbetweensoil temperatureand other
growth-limiting
factorsto illustratehow simple generalizationsabout temperatureand root functioningcan be
misleading.
Key words: roots,temperature,respiration,carbon,nutrients,water,atmosphericCO2.
INTRODUCTION
Soil temperaturecan influence root growth, including the initiationand cessation of growth,cell
elongation, root length and diameter extension,
initiationof new lateral roots, and root branching
patterns (Kasper & Bland, 1992; McMichael &
Burke,1998). Warmersoil temperaturesoftenresult
in higherratesof root respirationand ion uptake if
otherfactors,such as lightand drought,do not limit
the physiologicalactivityof plants (Oertli, 1996;
Burtonet al., 1998; BassiriRad,2000). Rates of root
mortality
also seem to increasewithsoil temperature
(Forbes et al., 1997; King et al., 1999), and the flux
of C fromplant roots into the soil foodweb might
increase if global temperaturesrise as predicted
(Houghton et al., 1996).
*Authorforcorrespondence(tel + 1 906 487 2396; fax + 1 906
487 2915; e-mail [email protected]).
Changes in soil temperatureinteractwithchanges
in otheressentialresources.For example,bothwater
and nutrientavailabilityoftencovarywith changes
in soil temperature.Higher soil temperaturesresult
in increasednitrogen(N) mineralizationifsoil water
potentialdoes not limitmicrobialactivity(Piatek &
Allen, 1999; Zak et al., 1999). However, drought
conditionsoftenoccur when soil temperaturesare
relativelyhigh (Kuhns et al., 1985; Piatek & Allen,
1999). Interpretation of root-soil-temperature
responses are complicated by these types of environmentalinteraction.Furthermore,
soil temperature can affect photosynthesis, and as soil
temperaturesand photosynthesisincreasetogether,
changesin whole-plantsource-sinkrelationshipscan
occur (Lippu & Puttonen,1991; Landhausseret al.,
1996). For example,low soil temperaturescan limit
rates of enzymicallydriven root processes such as
growth,nutrientuptake,and respiration,decreasing
the demand for C and resulting in a negative
106
REVIEW
K. S. Pregitzer
et al.
25
(a)
20 -
5 cm
1 cm
-
10cm
20 cm
-
ax
Qr
E 40-
(b)
Cl)
35__
__
__
__
10
25cm
~~~~
~~~~1
10-
28 May
4 June
10cm
5cm
-
20 cm
11June
18 June
Fig. 1. Soil temperatureprofilesin a Michigan northernhardwoodforestdominatedby sugar maple (a) and
beneathindividualjuniper treesin an open pinyon-juniperwoodland (b) at the Sevilletalong-termecological
research(LTER) site in New Mexico, USA. Soil temperaturesforthe period 28 May to 18 June 1999 were
recordedevery30 min with HOBO H-8 dataloggers(Onset ComputerCorporation,Bourne, MA, USA).
feedback to photosynthesisthrough the accumulation of nonstructuralcarbohydrates in leaves
(Thomas & Strain,1991).
The search for generalizationsabout how soil
temperatureregulates root functioningmust be
tempered by the realization that differentpopulations of plants have evolved to cope with a wide
range of fieldtemperatureregimes.We know that
temperaturehas an importantrole in regulating
aboveground physiology and there are obvious
questionsthatneed to be addressedbelowgroundat
various taxonomiclevels: life form,genus, species,
and genotype.Finally,the age (ontogeny)of a plant
can also influenceresponsesof rootsto changingsoil
temperatures.Young perennial plants invest relativelymore C in tissue construction,whereasolder
plantsallocatea greaterproportionof theirannual C
budgetto themaintenanceoftherootsystemand the
replacementof short-livedfeederroots. We should
be carefulof generalizationsderivedfromlaboratory
experimentsthat can sometimesonly be conducted
on youngplants,especiallyin the case of long-lived
perennials.
The objectiveof thispaper is to reviewpublished
workon the responsesof finerootsto changingsoil
temperatures,so as to provide a synthesisof our
REVIEW
Responsesoffinerootsto temperature
currentunderstandingon belowgroundresponsesto
a warmingplanet,and targetimportanthypotheses
for future study. We examine the relationships
between soil temperature,root growth,root mortality, root respirationand photosynthesisto illustratewhat is known about responses of smalldiameter tree roots to temperature.The way in
which soil temperatureinteracts with other environmentalfactorsto influenceroot functioningis
emphasized in an attempt to avoid simple
generalizationsthatoftenconfoundour understanding of how temperatureinfluencesbelowground
processes. We also bring togetherpublished data
witha simulationof the exhaustionof nonstructural
carbohydratesas a way of bounding the potential
influenceof temperatureon root life span in the
absence ofacclimationofrespirationto changingsoil
Our focusis on finerootsand nottheir
temperatures.
associated mycorrhizas.Clearly, roots and mycorrhizas are intimatelyrelatedin termsof both form
and function(Allen, 1992). Nevertheless, a discussion of mycorrhizalresponses to changing soil
temperatureregimes is beyond the scope of this
paper (but see Fitteret al., 2000). We also do not
discuss the temperatureresponses of large, longlived, structuraland/orstorageroots.
SOIL
TEMPERATURE
IN
NATURAL
107
occur (Hendrick & Pregitzer,1996), can be quite
dynamic (Fig. 1). Temperature fluctuationsare
greatlydampenedwithdepth,and hourlyand daily
averagetemperaturesare similarat 10-20 cm in the
soil in Michigan, but less so in New Mexico. In
manyplant communities,a large proportionof fine
roots occurs near the soil surface,wherevariability
in soil temperaturecan be high over relativelyshort
periods of time.
Nutrientavailabilitytypicallyincreases with increasingsoil temperaturebecause the mineralization
of organicallybound nutrientsis directlyrelatedto
thetemperature-dependent
metabolicactivityofsoil
microbes(Shaver et al., 1992; Chapin et al., 1995;
MacDonald etal., 1995; Piatek& Allen,1999; Zak et
al., 1999). By contrast,it is very common for the
highestlevels of soil moisturestressto be associated
with high soil temperatures(Teskey & Hinkley,
1981; Piatek & Allen, 1999). Midsummerdroughts
oftencome at a timewhensoil temperatures
are at or
near their seasonal peak. Responses of roots to
changes in soil temperatureobviously have the
potential to be confounded by root responses to
concomitant changes in soil nutrient and water
availability.Clearly,fieldenvironmentscan be very
differentfromthe simple experimentalconditions
that are sometimesused to make predictionsabout
root responsesto soil temperature.
ENVIRONMENTS
In temperate,boreal,alpine and arcticsoils, average
temperaturesat a given depth generallyincrease
fromspringtomid-summerand thenbegiintodecline.
This seasonal patternhas been widelyreportedand
varieswithlatitude,elevation,topographicposition,
soil properties,soil drainage, and vegetationtype.
Soils also warmto progressivedepthsas thegrowing
season ensues (Kasper & Bland, 1992), again
dependingon soil propertiesand vegetation.At high
latitudes,soils can be eithertoo cold or permanently
frozenclose to the surface,inhibitingrootactivityat
certainsoil depthsthroughoutthe year.
One importantand oftenoverlookedaspect of soil
temperatureis short-termvariability. Near the
surface,soil temperaturecan fluctuatewidely,again
of the
dependingon the locationand characteristics
vegetationand soil (Fig. 1). We have foundthatsoil
temperaturesbeneath individual juniper trees in
New Mexico can fluctuateby > 10C on hourlytime
scales 1 cm beneaththe soil surface;even at a depth
of 5 cm, temperaturesare highlydynamic(Fig. 1).
The inter-spaces between plants in this open
pinyon-juniperwoodland exhibit even more remarkableshort-term
fluctuations
in soil temperature
to the point that we suspect that the surface5 cm
of soil in the inter-spaces are inhospitable for
root growth.Even under a very dense canopy in a
mesic northernMichigan sugar maple forest,soil
temperatures
near the surface,wheremostfineroots
ROOT
GROWTH
Considerable evidence suggests that the rate of
extensionin root lengthis positivelyrelatedto soil
temperature,all other factorsbeing equal. Roots
grow fasterat highertemperaturesin annual crop
plants (Kasper & Bland, 1992) and perennials
(Larson, 1970; Wilcox & Ganmore-Neumann,1975;
Teskey & Hinkley,1981; Bevington& Castle, 1985;
Kuhns et al., 1985; Lieffers& Rothwell, 1986;
McMichael & Burke, 1998; King et al., 1999;
Weltzin et al., 2000). Many of these observations
have come from controlled growth-chamberand
glasshousestudies,but fieldexperimentsand observationalstudies reportsimilarresults.Agronomists
have modeled root growthwith depth by using the
rate at which soils warm progressivelywith depth
throughoutthespringand summer(Kasper & Bland,
1992).
Controlledexperimentsalso demonstrateoptimal
temperaturesforrootlengthextension,withgrowth
ratesacceleratingup to an optimumtemperature
and
then declining at supraoptimal temperatures
(Barney,1951; Merritt,1968; McMichael & Burke,
1998). Optimaltemperatures
forrootgrowthseemto
vary widely between differenttaxa, apparently
dependingpartlyon the inherentnativetemperature
regime (Larson, 1970; Tryon & Chapin, 1983;
McMichael & Burke, 1998). Nutrientuptake per
unit root length also increases with increasing
108
REVIEW
K. S. Pregitzeret al.
temperatureif plant growthis not limitedby other expansion.In deciduoustreesand shrubs,anyspring
factors(BassiriRad et al., 1993; BassiriRad, 2000). root growth that preceded the development of
These results are certainlynot surprising,given photosynthetically
functionalnew leaves would have
what we know about the relationship between to be fueledby theutilizationofstorednonstructural
temperature, photosynthesis and shoot growth carbohydrates.
(Beyschlag et al., 1993; Schwartz et al., 1997).
The breakingof dormancyand the development
However, as Fitteret al. (1998) recentlydiscussed, of new shoots is directly related to increasing
there is sometimeslittle correlationbetween field temperaturein most temperateand boreal plants
temperaturesand root growth. This is almost (Cannell, 1997; Barnes et al., 1998). Shoot decertainlyrelated to inherentannual (phenological) velopmentcan be predictedwithgreataccuracyfrom
patternsofgrowthand development,and limitations cumulative heat sum in the spring, and natural
imposed on the plant by other growth-limiting populations within a species exhibit genetically
resourcesabove and below ground.
controlled patterns of heat sum requirementsin
Changes in bothmoistureand nutrientavailability order for shoots to develop. By contrast, leaf
can also drive changes in root growth. Drought senescencein trees seems to be stronglycontrolled
clearlycauses a decrease in the rate of root length by photoperiod(Morgenstern,1996). The periodiextension(Rogers, 1939; Merritt,1968; Kaufmann, city of shoot growthand developmentin relation
1977; Deans, 1979; Teskey & Hinkley, 1981; to temperatureand day lengthis so well established
Bevington & Castle, 1985; Kuhns et al., 1985; forsome species of treesthatit is possible to predict
Kramer & Boyer, 1995), and droughtlowers con- how certainprovenanceswill behave even afterthey
ductance and canopy assimilation.When high soil have been relocatedfromtheirgeographicpoint of
temperatures are associated with conditions of originto anotherlocation with a different
temperdrought,there is no de facto reason to expect root ature and photoperiodic regime (Morgenstern,
growth to increase as soil temperaturesrise. An 1996). At presentwe do notunderstandwhetherroot
increase in soil N availabilitycan also cause an growthin thespringand rootmortality
in thefallare
increasein therateofrootlengthextension(Pregitzer related to the same environmentalcues that drive
et al., 1995; King et al., 1999; Pregitzeret al., 2000). shoot developmentand senescence. In temperate
Because N mineralizationincreases as soils warm deciduous treeswithhighlydeterminantpatternsof
(MacDonald et al., 1995; Piatek& Allen, 1999), it is shoot development,such as sugar maple, fine-root
importantto rememberthat root growthmightbe growth and mortalityseem to be much more
respondingto multiplesoil factorsthatcovaryas soil continuousand plastic than shoot growthand leaf
senescence (Hendrick & Pregitzer, 1992, 1993a,
temperaturesincrease.
1996).
The strong flush of root growth in the spring
SEASONAL
PHENOLOGY
means that considerable root production occurs
Although observational studies clearly document when soils are still relativelycool. For example,
both new root lengthextensionand root mortality Hendrick & Pregitzer(1996) reportedthat almost
throughout the growing season (Hendrick & 25% of sugar maple's annual root growthoccurred
Pregitzer,1992), perennialplants exhibita strongly beforeJuliandate 140 (20 May), a periodwhen soils
seasonal patternof new root productionand root are still cool. Fitter et al. (1998), studying an
witha burstof productionin spring,and elevationgradient,reportedthattheinitiationofroot
mortality,
laterat higher
significant
mortalityin the fall (Kuhns et al., 1985; growthin thespringwas progressively
Hendrick & Pregitzer, 1993a, 1996; Wells & elevations.Presumably,rootgrowthis initiatedlater
Eissenstat, 2000). This seasonal patternseems to at high elevationsbecause the soil warms at a later
correspondroughlyto leaf duration. In temperate date. It seems entirelypossible thatthe initiationof
forests,the most significantperiod of root growth root growth in the spring might be related to
correspondsto canopy developmentin the spring cumulativeheat sum in the soil and thatrootgrowth
and the most significantperiod of root mortality is synchronizedwith,but lags behind,shoot growth
corresponds to canopy senescence in the fall (Lyr & Hoffmann,1967). This hypothesisneeds to
(McClaugherty et al., 1982; Kurtz & Kimmins, be tested. If soil temperaturesat a given location
1987; Hendrick & Pregitzer,1992, 1993a, 1996). warmowingto human-inducedclimatechange,root
Root-shoot phenologicalobservationsof temperate growthwill probablybegin earlierin the year. The
(Arftet al., 1999)
treespresentedby Lyr & Hoffmann(1967) suggest International
TundraExperiment
that most of the flush of fine-rootgrowthin the and otherhigh-elevationand high-latituderesearch
spring might occur after canopy development. (Chapin & Shaver, 1996; Price & Waser, 1998)
However, detailed root-shoot physiological and clearlydemonstratethatshootgrowthbegins earlier
phenologicalobservationsare lackingand we simply in the Northern Hemisphere as air temperatures
do notunderstandwhetherrootgrowthin thespring increase,but comparable experimentalroot studies
precedes,correspondsto, or postdatesshootand leaf have never been conducted. A very interesting
REVIEW
Responses offine roots to temperature
question is whether or not all the meristems in a
perennial plant (i.e. shoots and roots) respond to
increasing spring temperatures in the same
genetically controlled way. If this were true, then
root growth would lag behind shoot growth in all
perennial plants because soils warm later than the
atmosphere in the spring.
ROOT
MORTALITY
Most of the extant root length in any perennial plant
is dominated by short lateral roots (Weaver, 1958;
Pregitzer et al., 1997, 2000). Presumably, main
root axes persist for much longer than lateral roots,
which grow and die in response to changing soil
environmental conditions (Pregitzer et al., 1997).
Little is known about the relationship between the
form of the absorbing root system and its function.
Wells & Eissenstat (2000) have recently demonstrated that larger-diameter 'fine roots' have longer
life expectances than smaller-diameter 'fine roots,'
raising the possibility that root longevity is related to
position on the branching root system. We do not
know how soil temperatures might impact the
interactions between root branching and root longevity.
How does increasing soil temperature influence
the rate of production and mortality of individual
fine roots? Hendrick & Pregitzer (1993b) observed
that fine-root longevity was shorter on sites where
soil temperatures were higher, but until recently the
role of temperature in regulating root life span has
received very little experimental attention. Forbes et
al. (1997), studying ryegrass (Lolium perenne var.
Parcour) roots, maintained plants in pots at 14, 21
and 27?C. They found that plants at the highest
temperatures maintained less root length, and that
individual roots had shorter life spans. King et al.
(1999) found that seasonally elevated soil temperature increased both the production and the mortality
of fine-root length in trembling aspen (Populus
tremuloides),with greater proportional increases in
production resulting in greater net root length
production (production-mortality).
Although the experimental evidence is very limited, the response so far has been consistent. Rates of
fine-root length extension and fine-root mortality
increase when soils warm. These results suggest
that, if other factors are equal, the growth of new
roots and the death of existing roots are accelerated
as soils warm. Such a conclusion must be tempered
by a deeper understanding of how soil temperature
influences seasonal root growth phenology, rates of
root respiration, whole-plant source-sink relationships, and the realization that there have not been
many experiments designed to understand the
interactions between soil temperature, soil moisture,
soil nutrient availability, and root growth and
mortality.
109
Extremely low soil temperatures also have the
potential to kill fine roots. In Alaska, considerable
fine-rootmortalitymight be associated with verv low
soil temperatures (R. Ruess, pers. comm.). Perennial
plants might have to rebuild absorbing root length
lost to freezing,a C cost that could vary considerablv
from year to year depending on snow cover and
climate variability. The interactions between low
soil temperatures and root growth have not been
extensively studied in natural ecosystems (but see
Tryon & Chapin, 1983), and there are potentially
important questions to resolve. For example, if
global warming causes boreal and arctic soils to have
higher minimum temperatures, warm faster in the
spring, or warm to a greater depth, then patterns of
root growth and mortality, and C allocation to root
systems, can be expected to change. Simple conceptual or empirical models of the relationships
between changing soil temperatures and root growth
and mortality are probably inadequate to predict
root responses in the future.
ROOT
MORPHOLOGY
AND
TISSUE
QUALITY
Soil temperature also has the potential to alter the
morphology and tissue quality of the absorbing
roots. Kasper & Bland (1992) have reported a
positive relationship between accumulated meristem
temperature and the number of lateral roots in crop
monocots. By contrast, Wilcox & GanmoreNeumann (1975) have reported that high soil
temperatures (27?C) result in fewer lateral branches
in red pine (Pinus resinosa) than lower soil temperatures (16 and 21?C). In general, there are few
investigations of the influence of soil temperature on
root morphology. If soil temperature alters nutrient
availability or rates of diffusionof nutrients to roots,
a change in root morphology might ensue. Little
research has focused on how soil temperature alters
root tissue qualitv (King et al., 1996), but root tissue
quality might have a kev role in regulating how
microbial communities respond to a changing global
environment (Zak et al., 2000).
ROOT
RESPIRATION
Higher temperatures generally result in increased
rates of root respiration, and the relationship between rates of respiration and temperature has been
widely reported to be exponential. It is often
assumed that Ql0 values are 2.0, that is, respiration
rates double for every 10?C increase in temperature.
However, there is actually a rather wide range in
reported Q10 values for roots of tree species, with
most values ranging from 2 to 3 (2.7 (Cox, 1975),
1.9-2.1 (Cropper & Gholz, 1991), 1.5-3.0 (Lawrence
& Oechel, 1983), 2.0 (Sowell & Spomer, 1986), 2.7
(Burton et al., 1996), 2.1 (Zogg et al., 1996), 2.0
(Ryan et al., 1996), and 2.0 (Bouma et al., 1997)).
110
REVIEW K. S. Pregitzeret al.
Some of this variationmightresultfromthe use of soil is warm and moist. All three factors (soil
different
experimentaldesigns by different
investi- temperature,water and N availability) have the
gators. It is knownthat Q10can varydependingon potentialto change togetherin the fieldand all can
therangeoftemperatures
overwhichitis determined directlyinfluenceratesof root respiration.We need
(Lawrence & Oechel, 1983; Ryan,1991), withhigher carefullydesigned field experimentsto clarifythe
values of Q10occurringwhen low (cold) temperature influencesofmoistureavailability,N availabilityand
rangesare examined.
soil temperatureon ratesof root respiration.
One of the most significantquestions yet to be
resolvedis whetherratesofrootrespirationacclimate
OF
SIMULATION
OF UTILIZATION
to soil temperature.Our laboratorystudiesof sugar
BY USING
CARBOHYDRATES
NONSTRUCTURAL
maple suggestthatfinerootsof this species respond
AND ROOT
MOISTURE
FIELD
TEMPERATURE,
in a generallysimilarwayto increasesin temperature
NITROGEN
CONCENTRATIONS
throughoutthe growing season, and little temperature acclimation occurs (Burton et al., 1996, How long could thefinerootsof sugarmaple respire
1998; Zogg et al., 1996). For whitespruce,Weger & without any new nonstructural carbohydrates
Guy (1991) also found no evidence that root (TNC)? Using actual field measurementsof soil
respirationacclimatedto temperature.Similarly,no temperature,soil matricpotentialand root tissue N
evidenceof temperatureacclimationhas been found concentrations,we conducted a simple simulation
for root respiraton in Engelmann spruce (Picea exercise to explore this question. We assumed no
engelmannii)or subalpine fir (Abies lasiocarpa; acclimation to temperature;our studies of sugar
Sowell & Spomer, 1986). However, Bryla et al. maple up to thispointsuggestthatlittleacclimation
(1997) foundthat,in citrusseedlings,rootrespiration to temperatureoccurs (Burton et al., 1996, 1998;
acclimated to temperaturewithin 4 d after the Zogg et al., 1996). However, we have reported
temperatureof the root systemwas changed to a evidenceforreducedratesof fine-rootrespirationin
different
constanttemperature.Korner & Larcher sugar maple during drought(Burton et al., 1998).
(1988) and Fitter et al. (1998) have also reported The purpose of the simulation was to establish
evidence for the acclimationof root respirationto boundaryconditionsforrootlifespan based on TNC
temperature.It could be that species differin their concentrations,and field temperature,moisture
abilityto acclimateto temperature.It is also possible and root tissue N conditions. By focusingon the
thatnear-constanttemperaturesare needed to cause exhaustion of TNC at ambient field conditions
acclimation,and thatthenaturaldiurnaland seasonal during differenttimes of the year, the potential
fluctuations
thatoccurin temperate importanceof acclimation and/or import of new
soil-temperature
and boreal ecosystemsmightpreventacclimationto TNC to roots would, it was hoped, become more
anylargedegreein thefield.As Fig. 1 demonstrates, apparent.Our detailedfieldand laboratorystudiesof
field temperaturescan fluctuate significantlyon fine-rootrespirationin sugarmaple acrossa rangeof
hourlyand daily timescales, especiallynear the soil field temperatures,combined with a program of
surface, where roots are concentrated in many continuous soil temperatureand matric potential
ecosystems.Step experimentsin whichtemperatures monitoring,providedthe necessaryset of measureare controlledat different
constantset pointsdo not mentsforconductingthe simulation.
accuratelymimicfieldconditionsin manyinstances.
We surveyedthe literatureto determinethe range
The issue of rootrespirationacclimatingto different in concentration
ofTNC in thefinerootsoftrees.In
temperaturescertainlydeservesmore attentionuntil general, the fine roots of trees are 4-6% TNC,
the contradictoryevidence is resolved and the rangingto as high as 20% TNC (Table 1). Using
mechanismscontrollingroot acclimationare under- actual fieldtemperaturesand an empiricalrelationstood (Atkinet al., 2000).
ship that predicts fine-rootrespirationfrom soil
It is worth noting that limited evidence clearly temperature,soil matricpotentialand root tissue N
we simulatedthe exhaustionof TNC
supports the notion that root respiration slows concentration,
(acclimates) during drought (Bryla et al., 1997; reservesat 1 % TNC incrementsfrom1% to 150%
Burton et al., 1998). Because field soils are often TNC, which includes most of the range of TNC
warm and dry at the same time, the effectsof soil concentrations
reportedin Table 1. The approximate
temperatureand droughton ratesofrootrespiration time to exhaustionof C supply assumed that there
could easilybe confounded.It is also clear thatrates was no temperatureacclimationoverthe durationof
of root respirationare directlyrelated to tissue N the simulation,that no new nonstructuralcarbocontent(Ryan, 1991; Ryan et al., 1996; Pregitzeret hydratewas translocatedinto the fine roots, that
al., 1998). Because the respirationof plant roots is 10000 of the TNC in rootswas available to support
directlyrelatedto N concentration,
it is possiblethat maintenancerespirationof existingindividualroots,
increases in root respirationat high temperatures and thatTNC (sugar plus starch)is approx.40?/oC.
might be due in part to higher rates of N This simple hypotheticalexercise was designed to
mineralization,whichwould be promotedwhen the enable us to begin to understandhow long it was
REVIEW
Responsesoffinerootsto temperature
111
Table 1. Percentagesoftotalnonstructural
carbohydrates
(TNC) infinerootsfromvarioussourcesin theUSA
TNC
(starches
+ sugars)(%)
Rootdiameter
(mm)
Species
-8-14*
4-6 solublesugars
8-12 TNC
1.6-8.5
8.5-15
-2.5-0.4:t
2-20 (most<10)
-3.5-6?
Locationt
Reference
Pinustaeda
NC, OK, AK (fall-winter) Hallgrenetal. (1991)
Northern
WI (fall)
J. S. King,pers.comm.
Populustremuloides
Betulapapyria
Populusspp.
Clonesgrownin MI (fall) Nguyenetal. (1990)
Clonesgrownin MI (fall) Nguyenetal. (1990)
Populusspp.
Acersaccharum VT (springand fall)
Liu & Tyree(1997)
Picea sitchensis Scotland(May-Aug)
Ford& Deans (1977)
FL (fall,winterand spring) Eissenstat
Citrussinensis
&
Duncan(1992)
<<1
< 1
00.5
0.05-1
2
Variable
<2
*Estimated
visuallyfromFig. 1.
abbreviations.
tUS statenamesaregivenas thetwo-letter
tEstimated
visuallyfromhealthystandvaluesin Fig. 1.
visuallyfromunprunedFig. 1.
?Estimated
Locationsofsamplesand timingofsampling(in parentheses)
fromeachstudyareincluded.
and estimatedtime(wk) beforethe nonstructural
Table 2. Average weeklysoil temperature
carbohydrate
is existinig
(TNC) contentof sugarmaplefinerootsis exhaustedif theonlycarbonfor maintenance
respiration
TNC
SiteA
460 52' N, 880 53' W
Averageweeklysoil
Week18 Week32
temperature
(OC)
TNC (O)8.60C
1
2
3
4
5
6
7
17.O0C
<1
<1
<1
<1
1
1-1.5
1-1.5
8
9
10
1.5-2
2
2-2.5
13
2.5-3
11
12
14
15
2.5-3
2.5-3
3-3.5
3-3.5
<1
<1
<1
<1
<1
< 1
< 1
<
1
1-1.5
1-1.5
SiteB
Site C
440 23' N, 850 50' W
430
Week18 Week32
Week18 Week32
10O.00C
18.30C
Week18
Week32
<1
<1
<1
<1
1
1
<1
<1
<1
<1
<1
<1
<1
<1
<1
<1
< 1
< 1
<1
1-1.5
1-1.5
<1
< 1
< 1
8.70C
17.30C
<.
<I
1-1.5
1.5-2
1.5-2
1.5-2
1.5-2
2
1
< 1
< 1
<1
<1
1-1.5
1-1.5
1.5-2
1.5-2
1.5-2
<1
1
1-1.5
1-1.5
1.5-2
1.5-2
1.5-2
1.5-2
1.5-2
2-2.5
2-2.5
2
2-2.5
2
2-2.5
1.5-2
2-2.5
2.5
2.5-3
2.5
2.5-3
2.5-3
2.5-3
1.5-2
Site D
40' N, 860 09' W
450 33' N, 840 51 W
2-2.5
2-2.5
2-2.5
<1
<
<
1
1
1-1.5
11.10C
<1
1.5-2
1.5-2
1.5-2
1-1.5
1-1.5
1.5-2
2-2.5
1-1.5
1.5-2
2-2.5
2-2.5
1-1.5
2-2.5
18.80C
<1
<
<
<
1
1
1
< 1
1
1-1.5
1-1.5
1-1.5
Ratesofrespiration
atthebeginnings
ofweek18(1 May1998)andweek32 (7 Aug1998)
(g C g-1wtwk-1)wereestimated
and used to calculatethe lengthof timethatit wouldtaketo exhaustTNC reserves(see the textfordetailsand
assumptions).
possible forfinerootspotentiallyto survivewithout
the importof new C fromthe canopy or reserveC
storedelsewherein the tree.
The root respirationsimulationused daily mean
soil temperatures(depth 15 cm) and dailymean soil
moisturelevels (depth 15 cm), whichwere recorded
in four northernhardwood stands during 1998
(Brownet al., 2000). The fourstandsextendalong a
500-km latitudinal gradient from northern to
southernMichigan (see Burton et al. (1996) for a
map of site locations and stand attributes).Yearly
precipitationis fairlyconsistentamong the sites;
however,themean annual air temperaturedecreases
fromthe southernto the northernsites (Burton et
al., 1996).
The followingempiricalrelationshipfromBurton
et al. (1998) was used to estimateroot respiration
rates:
Rco =(0.058N+0.622M)e0.098T
Eqn 1
(RC02 the respirationin nmol CO2 g-1 fine-root
biomass s-1; N, the root N concentrationin g kg-';
M, soil matric potential in Mpa; T, the soil
at 15 cm.) The relationshippresentedin
temperature
Eqn 1 accuratelyrepresentedrootrespirationacross
all foursites,and therewas no apparentevidenceof
temperatureacclimation(Burtonet al., 1996, 1998).
Eqn 1 was used to estimate weekly fine-root
respiration(g C g-1rootwk-1)forsitesA-D forthe
weeksof 1 May and 7 August1998. The averageroot
112
REVIEW
K. S. Pregitzeret al.
N concentrationused in the calculationswas based
on the measurementof rootspreviouslycollectedat
each studysite (site A, 17.4 g N kg-1;site B, 18.8 g
N kg-1; site C, 18.6 g N kg-1;site D, 17.4 g N kg-1
(Burton et al., 1996)).
The resultsfromthe simulationexerciseare quite
revealing.Given our assumptions,finerootsofsugar
maple can live only a matterof weeks in August
withoutnew C, regardlessof their TNC concentration(Table 2). Typical TNC concentrationsof
4-6% resultin the consumptionof all the TNC in
fine roots in <1.5 wk in August at ambient soil
temperatureand soil matric potential (Table 2).
Even duringMay, when soil temperaturesare still
relativelycool, we estimatedthat4-6% TNC would
be gone in <2 wk (Table 2). These resultsclearly
demonstratetwo importantpoints. First, understandingacclimationand how the process worksis
critical,because withoutacclimationto temperature,
rootlifespans mustdepend on the continualimport
of new TNC, even in the short term. Second, it
seems very likelythat during the growingseason,
whenthereare manyactivelygrowingrootand shoot
meristems,rates of fine-rootrespirationand root
longevitymightbe closelylinkedto ratesof photosynthesisand whole-plantsource-sinkrelationships.
As we discuss later,thereis alreadylimitedevidence
forthis second conclusion.
WHOLE-PLANT
SOURCE-SINK
RELATIONSHIPS
In a studyof whole-treeC allocationwithspecial
emphasis on the quantificationof C allocation to
roots and root respiration,Horwath et al. (1994)
labeled a blockof 3.0-m-tallhybridpoplars(Populus
euramericanacv. Eugenei) with14CO2in Julyand in
September. They found that the "'C specific
radioactivityof soil respirationpeaked 2 d afterthe
addition of 14CO2 in both July and September.
During July,activelygrowingshoots are a much
than in September,
strongersink forphotosynthate
when, afterbudset, most of the C assimilatedby
these genotypesis translocatedto the root system
(Dickson & Nelson, 1982; Pregitzeret al., 1990). In
both July and September,most 14C had respired
from the soil within 100 h of canopy labeling,
stronglyindicatingthat root respirationis tightly
coupled with canopy assimilation, regardless of
whole-treesource-sinkrelationships.If this is true
in most field situations,then root respirationand
perhapsfine-rootlongevityshould be linkedto rates
of canopy C assimilation. However, several key
questions remainunresolved.
* How tightlycoupled are canopy assimilationand
timesof the yearand
rootrespirationat different
duringperiods of stressthatalterroot and shoot
function?
* How long does it takefortherootsystemto begin
to utilize stored nonstructuralcarbohydrates
when environmentalstressresultsin littleor no
photosynthesis,and how long can roots survive
on storedcarbohydrates?
* Is the primarymode of coping with stress the
down-regulationof fine-rootrespiration,or do
some taxa shed rootsduringperiods of stress?
How interdependentare the roots and shoots of
perennial plants? This question is relevant to
understandingthe responsesof roots to changes in
temperatureand our simulationsuggeststhat root
and shoot activitymight be very tightlycoupled The Horwath et al. (1994) 14C labeling experiment
during the growingseason. It seems clear that in withtrees,and shadingexperimentswith perennial
some herbaceous plants, photosynthesisand root grasses (Bilbrough& Caldwell, 1995), both suggest
respirationare directlycoupled on time scales that thatfine-rootrespirationis closelylinkedto canopy
range from minutes to hours (Hansen, 1977; assimilation.We expectthatthiswould be especially
Massimino et al., 1981; Ryle et al., 1985; Amthor, true during the growing season, when there are
1994). Afterreviewingworkwithannual plantsand hundreds to thousands of active meristemsat the
conductingexperimentswithsingle-rootedsoybean whole-treelevel and sink strengthis high at manyleaves, Farrar& Jones(2000) arguethatC allocation locationswithinthetree.Fitteret al. (1998) recently
to roots is controlledjointly by roots and shoots. reportedthat root respirationalong an elevational
However,the relationshipsbetweenphotosynthesis, gradientof grasslandswas most closely correlated
C allocationto roots,and ratesofrootrespirationare withprecedingradiation,also suggestingthatcanopy
not well understoodin trees and shrubs,which are assimilationand root respirationmight be tightly
much larger and longer-livedthan annual plants. linkedin grasslands.In general,we hypothesizethat
The average velocity of sugar transportin tree ratesofrootrespirationare directlylinkedto ratesof
phloem tissue is only a few cm h- (Kozlowski & canopy assimilationin perennial plants, probably
Keller, 1966), and treesand shrubssometimeshave with time lags that are no longerthan a few days.
large TNC reserves(Waring & Schlesinger,1985), Any environmentalfactoralteringrates of wholeso it seems unwise simply to assume that the canopy assimilationwould eventuallyalso influence
mechanismscontrollingC allocationto rootsare the rootrespiration,
but thetimescales involvedarevery
same in annuals and perennials.Nevertheless,some poorly understoodin trees. This hypothesiscould
data fromtrees also suggesta strongand dynamic potentiallyexplainhow variableenvironmental
conlinkage between rates of canopy assimilationand ditionsregulaterootrespiration.If soil temperatures
the
increase,and waterand nutrientsare sufficient,
root respiration.
REVIEW
Responsesoffinerootsto temperature
113
rates of both canopy assimilation(Schwartz et al., productionand mortality,
and greaterroot C fluxto
1997) and root respirationincrease (Burton et al., the soil. The influenceof soil temperatureon root
1998). If soil temperaturesare high but drought functioningin boreal and tundra environments
inhibitsconductanceand assimilation,rates of root clearlyneeds additionalstudy.In thesecold regions
respiration decline. This hypothesis should be wherethe proportionalallocationof C to roots and
reasonablystraightforward
to test. If the hypothesis mycorrhizaeare highand C storageis great,surface
is not true, fine-rootrespirationover significant soil temperatures
musthave a keyrolein determining
periodsof decreasedphotosynthesis
mustdepend on when roots grow, how they functionand perhaps
stored nonstructuralcarbohydrates,implyingthat whether they die. Our simulations of fine-root
the root and shoot systemsare decoupled in timein respiration,and the limitedliterature,suggestthat
their response to changing environmentalcon- duringthegrowingseason finerootsmustdepend on
ditions, an unlikely scenario. The idea that root the import of new C to survive for even limited
respirationrapidly adjusts to temperaturein all periods. We hypothesize that rates of fine-root
situations seems overly simplistic. Factorial field respirationin summerare tightlycoupled withrates
experimentsthat create dynamic 'hot-wet' and of conductance and photosynthesis.However, the
'hot-dry' soil conditionsthatsignificantly
alterrates way in which soil temperature,soil water, soil
of conductance and photosynthesisshould prove nutrients and sunlight interact to control root
useful in understanding how root respiration respiration,root growthand root mortalityis very
respondsto temperatureas multiplegrowth-limiting poorlyunderstoodin large,perennialplants.
soil conditionschange during the growingseason
(Bilbrough& Caldwell, 1995).
ACKNOWLEDGEMENTS
It is importantto note thatwe do not have a clear
Fundingforthisresearch
wasprovided
bytheUS National
ofhow tightlycoupled in timecanopy
understanding
ScienceFoundation
(NSF grantsDIB 94-13407,DEB 96assimilationand rootfunctioning
are over the range
forEcosystem
29842andDEB 96-15509),DOE's Program
of environmentalconditions that perennial plants Research(DE-FG02-93ER6166),theUSDA ForestSertypically experience in the field. Gebauer & viceNorthern
GlobalChangeProgram,
andUS MclntireEhleringer(2000) recentlydemonstratedthat,in dry StennisActfunds.
waterand N uptake in shallow roots
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