Short note

Ecophysiological factors contributingto the distributions of several Quercus species

in the intermountain west

JR Ehleringer, SL Phillips

Department of Biology, University of Utah, Salt Lake City, UT 84112, USA

(Received 1 March 1995; accepted 1 November 1995)

Summary — Aspects of the water relations of three oak species (Quercus gambelii, Q turbinella andQ macrocarpa) and their hybrids (Q gambelii x turbinella, Q gambelii x macrocarpa) were observed undercommon garden conditions in northern Utah, USA. In the absence of summer moisture inputs, Qmacrocarpa and Q turbinella were unable to maintain active gas exchange through the day; followingan early morning peak, leaf conductances to water vapor remained very low through the remainder ofthe day. In contrast, Q gambelii and the hybrids were able to maintain high leaf conductances through-out this period. Consistent with these observations, Q gambelii is thought to have a root system pen-etrating to the deeper, winter-recharged layers, a feature apparently absent in both Q macrocarpa orQ turbinella. Based on current hybrid distributions, both Q turbinella and Q macrocarpa once extendedinto drier more northerly regions than they occupy at present. When these parents retreated, they leftbehind hybrids with Q gambelii, which do not depend on monsoonal moisture input. Leaf size, leaflongevity, carbon isotope ratio, and minimum winter temperatures appear not to be correlated withthe absence of Q macrocarpa and Q turbinella from summer-dry habitats. Instead it appears thatreliance on summer monsoon events is one of the critical factors influencing loss of these oaks fromsummer-dry sites in the intermountain west.

leaf conductance / monsoon / carbon isotope ratio / oak / Quercus

Résumé — Facteurs écophysiologiques contribuant à la distribution de différentes espèces dechênes dans l’Ouest américain. Les caractéristiques hydriques de trois espèces de chênes (Quer-cus gambelii, Q turbinella et Q macrocarpa) et de leurs hybrides (Q gambelii x turbinella, Q gambeliix macrocarpa) ont été analysées sur des arbres en plantations comparatives dans le nord de l’Utah(États-Unis). En l’absence d’irrigation pendant les mois d’été, Q turbinella et Q macrocarpa étaientincapables de maintenir des échanges gazeux actifs en cours de journée ; après un pic matinal, laconductance stomatique restait très faible pendant le reste du temps. En revanche, Q gambelii et leshybrides ont maintenu des conductances stomatiques élevées pendant toute cette période. Ces obser-vations sont à mettre en relation avec la présence sur les individus de Q gambelii d’un système raci-naire capable d’atteindre les couches du sol plus profondes et rechargées en humidité en cours de l’hi-

ver, alors que ni Q turbinella ni Q macrocarpa ne présentent cette caractéristique. En se basant sur ladistribution actuelle des deux hybrides, on peut supposer que Q turbinella et Q macrocarpa occu-paient autrefois des régions plus septentrionales et plus sèches que leur aire actuelle. Lors du retraitdes deux espèces parentes, les hybrides avec l’espèce Q turbinella, qui dépend moins des pluiesestivales, sont restés en place. La dimension et la longévité des feuilles, le rapport de composition iso-topique du carbone, et les températures hivernales minimales ne sont pas corrélés avec l’absence deQ macrocarpa et de Q turbinella des habitats à sécheresse estivale. En revanche, la dépendanceaux pluies estivales semble être le facteur critique contribuant à la disparition progressive de cesespèces des sites à sécheresse estivale de la zone des plateaux de l’ouest américain.

conductance stomatique / pluies estivales / composition isotopique en carbone / chêne /sécheresse

INTRODUCTION

Oak distributions have been influenced bynumerous abiotic and biotic factors over themillenia. Since the last glacial-interglacialcycle, there is substantial evidence frompollen analyses of lake sediments indicatingsignificant oak migrations in eastern por-tions of North America. In the Rocky Moun-tain and intermountain west portions of thewestern United States, pack rat middenrecords have recorded the migration of oaksand other woody species (Betancourt et al,1990; Cole, 1990). While general aspectsof the factors contributing to a species’migration may be derived from either pollenor midden analyses, specifics on the envi-ronmental factor(s) influencing the capac-ity of a species to invade or persist in a spe-cific habitat may be more elusive.

Relictual natural hybrids of oak speciesmay provide some insight for elucidatingwhy one particular oak has migrated awayfrom a geographic region that once wasoccupied by two or more oak species. Inthe western United States, numerous relictoak hybrid populations have been described,where one of the parents has retreatedsome 200-500 km from its original location.Such is the case for naturally occurringhybrids involving 1) Quercus gambelii and Qturbinella, and 2) Q gambelii and Q macro-carpa. Drobnik (1958) described Q gambe-lii x turbinella hybrids occurring at the lower

elevation limits of Q gambelii all along thewestern range of Q gambelii (fig 1). Cottamet al (1959) noted that these hybrids hadarisen since post-glacial periods and thoughtthat these hybrids represented long-livedremnants from former periods when the twospecies had overlapping distributions, per-haps as long as several thousands of yearsago. Since Drobnik’s original observations,hybrids between these two oaks have beencollected from additional locations in cen-

tral Utah, but there have been no firm ageestimates for any of these hybrid clones.

The two most common oak species in theRocky Mountain and intermountain west por-tions of the western United States are Q

gambelii and Q turbinella. While there isspecies overlap and frequent hybridizationat the southern portions of the distribution ofQ gambelii, the occurrence of long-livedhybrids between Q gambelii and Q turbinella300 km north of the northernmost Q turbinellais unusual and has been the focus of pale-oecological interest (Drobnik, 1958). Cottamet al (1959) proposed that cold winter tem-peratures were the primary factor restrictingthe distribution of Q turbinella to the southerlylatitudes and that these hybrids were rem-nants of a warmer postpluvial climate. Whilenot focusing specifically on the remnant oakhybrids, Neilson and Wullstein (1983) con-cluded that a combination of spring freezesand summer moisture stress restricted the

northerly distributions of both Q gambelii and

Q turbinella. In related studies, Neilson andWullstein (1985, 1986) showed that both oakspecies exhibited nearly identical water rela-tions and drought tolerance characteristicsand the oak seedling establishment occurredonly in the southern locations where sum-mer rains were frequent.A third oak species, common to habitats

with abundant summer precipitation, hasalso left behind hybrids, possibly also indica-tive of a previous wetter climate. Q macro-carpa is common throughout the easternportions of the Great Plains of North Amer-ica. However, remnant hybrid populationsof Q gambelii x macrocarpa occur in easternparts of both New Mexico and Wyoming, ator beyond the driest portions of the currentwestern limits of Q macrocarpa’s distribu-tion (Tucker and Maze, 1966; Maze, 1968).

The focus of this paper is to examine

aspects of the water relations of these threeoak species native to the intermountain westand of their hybrids under common growthenvironments in order to evaluate charac-teristics that might have been important inrestricting the distribution of one parent andyet allowing the hybrids to persist as one ofthe parents retreated from its former distri-bution.

Q GAMBELII, Q TURBINELLA,Q MACROCARPA, AND HYBRIDDISTRIBUTIONS

Q gambelii is widely distributed through theRocky Mountain region of North Americafrom northern Utah and Colorado in the northto southern Arizona and New Mexico in thesouth (fig 1). It is a dwarf tree, ranging inheight from 2 to 10 m. Ecologically, in itsnorthern distribution range this species occu-pies the scrub-brush zone between the lowerboundary of the white fir forest and the upperlimits of the sagebrush steppe, while in thesouth its distribution is between the juniperwoodland and pine forest communities.Nielsen and Wullstein (1983, 1985) charac-terized the biogeographic factors limiting thedistribution of Q gambelii; they concludedthat cold winter temperatures and springfreezes determined the northern distributionlimits of this species and that summer waterstress was a contributing factor limiting thisoak’s distribution.

Q turbinella has narrower and more

southerly distribution compared to Q gam-belii (fig 1). This oak is also a scrub oak,ranging in height from 2 to 5 m. Ecologically,its distribution is very similar to that of Q

gambelii, being a dominant component ofthe transition between arid zone scrub andconiferous woodland. Q turbinella tends to

grow in habitats with lower overall precipi-tation amounts than Q gambelii. Hybridscommonly occur where the distributionsoverlap in southern Utah and northern Ari-zona. Nielsen and Wullstein (1983, 1985)concluded that both cold winter tempera-tures and the northern extent of the Ari-zona summer monsoon limited the north-

ern distribution of Q turbinella.

Q macrocarpa is widely distributedthroughout the central states region of theUnited States and on into southern Canada

(fig 2). This oak is common along riparianregions and forms a tree that reaches amaximum height of 7 to 10 m. Its distributionis bounded on the east by the eastern decid-uous forest and on the west by the semi-arid grasslands of the Great Plains.

MATERIALS AND METHODS

Study site

Measurements were collected on parents and F1hybrids of oaks established in the Cottam Oak

Grove at the University of Utah (lat 40°46’, long110°50, 1 515 m). Soil at the site is alluvial andoccurs to a depth of 2-3 m. Q gambelii, Q macro-carpa, and Q turbinella were planted into the Cot-tam Oak Grove in the mid-1960s (Cottam et al,1982). Hybrids were produced by hand pollinationand acorns planted into the same experimentalgarden. All plants had been irrigated to get themestablished, but then watered sparingly in lateryears.

During the two summers of our investigations(1985 and 1994), these trees received very limitedsummer precipitation and no irrigation because ofirrigation-system failures; 1993 was a wetter andcooler year throughout the growing season. Oakswere also sampled at the Shields Grove Arbore-tum of the University of California at Davis (lat38°33’N, long 121 °44’W, 15 m elev), where Cot-tam and colleagues had also planted parents andhybrids from the same crosses (Tucker andBogert, 1973; Cottam et al, 1982).

Leaf conductance and transpiration

Leaf conductance and transpiration rates weremeasured with a steady state porometer (model1600, Licor Instr, Lincoln, NE, USA). Each valuerepresents the mean of five individual leavesmeasured on a single tree. The data presentedrepresent the means of three trees.

Leaf water potential

Predawn water potentials were measured on cuttwigs of oak parents and hybrids using a pres-sure chamber (PMS Instr, Corvallis, OR, USA).

Isotope ratio analyses

For carbon isotope ratios (δ13C), five sunlit leavesper tree were collected, combined to form a sin-

gle sample, oven-dried and finely ground. Thesesamples were prepared, combusted, and ana-lyzed using an isotope ratio mass spectrometer(model delta S, Finnigan MAT, San Jose, CA,USA) following procedures outlined in Ehleringer(1991). Leaf carbon isotope ratios (δ13C) areexpressed relative to the PDB standard; the over-

all analysis precision was ± 0.11‰. Water sourceutilization was estimated by measuring the hydro-gen isotope ratio of water in the xylem sap(Ehleringer and Dawson, 1992). A single suber-ized stem from each tree was collected and waterfrom this stem was extracted cryogenically undervacuum (Dawson and Ehleringer, 1993). Forhydrogen isotope ratios (δD) of xylem sap, waterwas converted to diatomic hydrogen using a zinc-mediated reaction (Coleman et al, 1982). Analy-ses were then made using the same mass spec-trometer as above with an overall analysisprecision for hydrogen of ±1‰ and are expressedrelative to the SMOW standard.

RESULTS

Parents and their F1 hybrids growing in theexperimental garden were first comparedfor differences in leaf size (table I). Whilethis morphological parameter has beenused historically as a reliable means of dis-tinguishing among parents and hybrids, itssignificance may be of adaptive value andinfluence plant distribution if leaf boundarylayer considerations are important in influ-encing water relations, leaf temperature, orother aspects of leaf metabolism and if thecharacter has limited variability. The decid-uous-leaved Q gambelii leaves were signif-icantly larger than those of either the ever-green-leaved Q turbinella or the tardilydeciduous Q gambelii x turbinella hybrids.Such leaf size differences would contributeto a larger boundary layer in both Q gambeliiand the hybrids, possibly a disadvantagefor plants if transpirational evaporative cool-ing was not possible to help reduce leaftemperatures. Yet, countering this is that itis the smaller-leaved Q turbinella which isthe species now absent from this summer-dry northern habitat; the larger-leaved Qgambelii and hybrids persisted in the northeven though summer rain is very limited.Differences in leaf size were maintained

throughout the growing season, despite theobservation that the leaf size of the second

flush of Q gambelii leaves was reduced by

41 %. Leaf mass-to-area ratios showed dif-ferences similar to the leaf size data (tableI). The evergreen-leaved Q turbinella hadthicker leaves than the deciduous-leaved

Q gambelii and the hybrids were consis-tently intermediate. Leaves of parents andhybrids tended to become thicker as theseason progressed.

Similar significant differences in leaf sizeand leaf mass-to-area ratios were alsoobserved between Q gambelii, Q macro-carpa, and their hybrids (table I). Q gam-belii x macrocarpa hybrid leaf sizes and leafmass-to-area ratios were similar to Q gam-belii early in the growing season and to Qmacrocarpa later in the season. In this com-

parison, the larger-leaved species (Q macro-carpa) would be expected to have higherleaf boundary layer (contributing to a higherleaf temperature) and this is the speciesthat occurs in habitats with summer rainsto relieve possible moisture stress. Thesemore traditional approaches provided lim-ited insight into the factors which might becontributing to distribution differencesbetween parents and the hybrids, eventhough comparisons were made under uni-form environmental conditions.

Based on the previous suggestion byNielsen and Wullstein (1983, 1985) thatsummer rain was critical to Q turbinella, wehypothesized that Q turbinella, which isabsent from the northern habitats, shouldbe more water stressed during the summerin the experimental garden than either Qgambelii or the hybrids. Under uniform soilconditions on nonirrigated plants in theexperimental garden, we evaluated waterstress in parents and their hybrids. Counterto our initial expectations, midday leaf waterpotentials during dry summers were morepositive in Q turbinella than in Q gambelii(fig 3) in 1985 and again in 1993 (data notshown). However, predawn leaf waterpotentials in both summers were more pos-itive in Q gambelii than in Q turbinella, sug-gesting that differences in midday water

potentials could have been the result ofstomatal closure. That is, stomatal closure inQ turbinella could have resulted in highermidday water potentials than in Q gambeliiand Q gambelii x turbinella, which may havecontinued to transpire and maintain steeperwater potential gradients between soil andleaf tissues.

Diurnal leaf conductance measurements

on Q gambelii, Q turbinella, and the hybridsrevealed that Q gambelii and Q gambelii xturbinella maintained substantially higherrates of gas exchange through the day thandid leaves of Q turbinella (fig 4). Gasexchange in Q gambelii and Q gambelii xturbinella leaves reached peak valuesshortly before midday and then declined astemperatures increased through the day.Leaf conductance in both Q gambelii andQ gambelii x turbinella was significantly cor-related with vapor pressure deficit (Q gam-

belii: r = -0.881, P < 0.01, Q gambelii x tur-binella: r = -0.688, P < 0.02). On the otherhand, following a peak value shortly aftersunrise, leaf conductances in Q turbinellaremained low throughout the day; however,these conductance values were still related

to vapor pressure deficit (r = -0.529, P <

0.07).Similar to Q turbinella, Q macrocarpa

naturally occurs in habitats with frequentsummer precipitation. On a separate date,the diurnal courses of leaf water potentialand leaf conductance were also measuredin Q gambelii, Q macrocarpa and Q gam-belii x macrocarpa to determine if the

absence of summer moisture inputs wouldresult in suppressed gas exchange and"apparently reduced" water stress patternssimilar to that observed for Q turbinella andits hybrids. Predawn leaf water potentialsin Q gambelii, Q macrocarpa and Q gam-

belii x macrocarpa were approximately thesame, but midday values were substantiallymore positive in Q macrocarapa than ineither Q gambelii or Q gambelii x macro-carpa in 1985 (fig 3) and again for both par-ents in 1993 (data not shown). The sup-pressed diurnal courses of leaf gas

exchange provided an explanation for theapparent midday reduction of water stress inQ macrocarpa. Higher rates of gasexchange occurred in Q gambelii and Qgambelii x macrocarpa than in Q macro-carpa, which had very much reduced leaf

conductances after attaining peak valuesin the early morning (fig 4). Leaf conduc-tances in all three were significantly corre-lated with leaf vapor pressure deficits: Q

gambelii (r = -0.903, P < 0.01), Q macro-carpa (r = -0.873, P < 0.01), and Q gam-belii x macrocarpa (r = -0.883, P < 0.01).

Together these gas exchange data indi-cated that both species native to habitatswith summer precipitation were not able tomaintain gas exchange through the day inthe experimental garden, which hadreceived no precipitation inputs since thelate spring. In contrast, the native species, Qgambelii, and the Q gambelii hybrids werealbe to maintain higher rates of gasexchange during this summer droughtperiod. These data are consistent with theidea that Q macrocarpa and Q turbinellawere more shallow rooted than Q gambeliiand that the F1 hybrids had rooting distri-butions similar to that of the Q gambelii par-ent.

To evaluate the possibility that oaks mightbe utilizing moisture from different soildepths during the summer months, waterpotentials and water sources of Q gambelii,Q turbinella, and hybrids growing in the Cot-tam garden were examined approximately 1week following a summer rain event in latesummer 1994. Predawn water potentials inQ gambelii were lower than in either Q tur-binella (-1.06 MPa vs -0.80 MPa, P < 0.10)or Q gambelii x turbinella (-1.06 MPa vs

-0.74 MPa, P < 0.04). However, the Q tur-binella and Q gambelii x turbinella shrubsdid not differ in their predawn water poten-tials (-0.80 MPa vs -0.74 MPa, P= 0.36). Atmidday, leaf water potentials in Q gambelii(-3.03 MPa) were still more negative than inQ turbinella (-2.72 MPa) at the P = 0.06level.

Consistent with this pattern, the hydro-gen isotope ratios (&delta;D) of xylem sap in theseoaks showed a tendency for Q gambelii(mean value of -130.1&permil;, range of -128 to131&permil;) to be using a more deuterium-depleted water source than Q turbinella(mean value of -123.5&permil;, range of -94 to- 130&permil;); however, this difference was onlysignificant at the P = 0.14 level because ofgreater variability in the responses of dif-ferent Q turbinella shrubs. Although &delta;D val-

ues of soil moisture throughout the soil pro-file were not measured to correlate with

xylem sap values, we would expect that thesurface soil layers would have a more pos-itive &delta;D value than deeper soil layers,because of evaporative enrichment andbecause summer precipitation has morepositive &delta;D values than the winter precipi-tation that charges the deeper soil layers(Phillips and Ehleringer, 1995).

Leaf carbon isotope ratio data were con-sistent with a pattern of functional rooting-depth differences among taxa. The springand summer of 1993 were among the

wettest and coolest periods in recent his-tory. Precipitation was well above long-termaverages at the Utah experimental garden.Leaf carbon isotope ratios measured on leafmaterials produced that year averaged near-27&permil; and no significant differences weredetectable among parental and hybrid mate-rials (table II). When these leaf carbon iso-tope ratio values were compared to valuesfrom parental and hybrid materials growingin an irrigated experimental garden at theUniversity of California at Davis, there wereno significant differences among taxa orbetween sites (table II). These results con-

trast with previous observations byEhleringer and Smedley (1989), indicatingthat leaf carbon isotope ratios were morepositive in Q macrocarpa and Q turbinellathan in Q gambelii. Yet leaf carbon isotoperatios for Q gambelii in that study were sim-ilar to those reported here. However, thoseearlier data were collected from plant mate-rials that had been growing under nonirri-gated conditions through a dry winter anddry summer in the same experimental gar-den. Leaf carbon isotope ratios representan integrated long-term estimate of the ratioof intercellular to ambient CO2 concentra-

tions and are known to be more positive forplants experiencing water stress (Farquharet al, 1989). Thus, water stress effects onleaf carbon isotope ratios manifested in aprevious study which had the typical sum-mer drought period (1985) were absentwhen taxa experienced limited water stress(1993).

DISCUSSION

Previous studies have concluded that theQ gambelii x turbinella and Q gambelii xmacrocarpa hybrids represent relicts fromprevious wetter periods (Maze, 1968;Nielsen and Wullstein, 1983). Both winter-spring temperatures (Cottam et al, 1959;Nielsen and Wullstein, 1983) and summerdrought (Nielsen and Wullstein, 1983) havebeen suggested as the factors pushing thenorthern boundary of Q turbinella south-ward. However, Q turbinella has been estab-lished in the Cottam Oak Grove at the Uni-

versity of Utah for approximately 30 years,and during that interval some of the lowestwinter and spring air temperatures of theprevious 150 years have been recorded (USWeather Bureau records). While cold tem-peratures may be an important factor limit-ing Q turbinella’s northern distribution, it is

likely that this factor is less critical than pre-viously suspected.

The persistence of Q gambelii x turbinellahybrids may be due to an increased capac-ity of these hybrids to utilize winter-derivedmoisture available in the deeper soil layerswhen soil moisture is absent from the sur-face layers. A clear differential utilization ofsurface versus deep soil moisture sourceshas been shown for Gambel’s oak. Phillipsand Ehleringer (1995) found that Q gam-belii in northern Utah utilized only moisturefrom deeper soil depths arising from winterrecharge events. Mature plants did not usemoisture from the upper soil layers followingsummer rain events. Our results are con-sistent with that pattern. In a parallel studyusing Mediterranean oaks, Valentini et al(1992) showed that the drought-deciduousQ cerris and Q pubescens used moisturefrom deeper depths. Again, these speciesdid not respond to and use summer mois-ture input, whereas the evergreen-leavedQ ilex utilized summer moisture. Our gas-exchange results indicate that Q turbinellalacks the deep rooting capacity which would

permit this species to remain active througha summer drought. The Q gambelii x tur-binella hybrids are either intermediate in thisrooting character or possess deeper rootsystems similar to Q gambelii. Since Q gam-belii and Q turbinella exhibit nearly identi-cal intrinsic water relations and drought-tol-erance characteristics (Nielsen and

Wullstein, 1985), the absence of summerrain on a predictable basis would then leadto the loss of Q turbinella from the northernhabitats if they are not able to maintain sum-mer gas-exchange activity on a regularbasis.

When did adequate amounts of summerprecipitation on a predictable basis disap-pear from the northern habitats now occu-

pied only by Q gambelii and Q gambelii xturbinella? Pack rat midden data indicatethat central and northern Utah had an exten-

sive summer-precipitation climate followingglacial retreat several thousand years ago,but the onset of regional summer droughtis less clear from these records. There is

evidence indicating pronounced shifts in cli-mate over the past several hundred years -shifts in both the amount and timing of pre-cipitation events. Stine (1994) observed thatseveral extended droughts of more than 100years occurred in the western United Statesearlier in this millennia. Feng and Epstein(1994) reported a shift in the hydrogen iso-tope ratios of bristlecone pine tree rings sev-eral hundred years ago, which is consistentwith a reduction in summer precipitation inthe Sierra Nevada Range. Coltrain (1994)reported that corn, once common, disap-peared from the diet of native Americansliving along the Wasatch Mountains of north-ern Utah approximately 700 years ago.Since corn is thought to have been culti-vated only in regions with summer rains,these data could indicate a loss of mon-

soonal precipitation along the northernWasatch Mountains. Lastly, Lanner (1974)reported hybrids of Pinus monosperma xedulis in the northern portions of the

Wasatch Range. Similar to Q turbinella, Pedulis now only occurs in habitats with reli-able summer precipitation. Since the near-est P edulis is approximately 200 km fromthe P monosperma x edulis hybrid popula-tions and since trees in this hybrid populationare less than 400 years old, these patternssuggest a relatively recent loss of reliablesummer moisture in the northern habitatsthat now have only the relictual hybrid oakand pi&ntilde;on pine populations.

The hybrid persistance of Q gambelii xturbinella, Q gambelii x macrocarpa, and Pmonosperma x edulis may be the result of

deeper rooting capacities that allow themto maintain gas-exchange activity througha prolonged summer drought. In a strictsense, the hybrids are likely all that remainfrom a recent historical period when the localregion had a reliable monsoonal moistureinput. While as a general pattern, mosthybrid plants occur in an intermediate habi-tat or microclimate with both parents sym-patric and persisting in the region, the oakand pi&ntilde;on pine hybrids describe relicts of aprevious climate where now only one of theparents has persisted. The use of parentaland hybrid oaks under common garden con-ditions allows us a means of teasing out thefactors that have contributed to the loss ofone parental species and therefore gain astronger insight into historical climatic pat-terns influencing plant distribution.

ACKNOWLEDGMENTS

We thank the National Science Foundation for

support of this research.

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