Temporal variation in temperature and rainfall differentially affects ectomycorrhizal colonization at two contrasting sites

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1 New Phytol. (1998), 139, Temporl vrition in temperture nd rinfll differentilly ffects ectomycorrhizl coloniztion t two contrsting sites BY RANDY L. SWATY*, CATHERINE A. GEHRING, MATT VAN ERT, TAD C. THEIMER, PAUL KEIM AND THOMAS G. WHITHAM Deprtment of Biologicl Sciences, Northern Arizon University, Box 564, Flgstff, AZ, 8611, USA (Received 9 December 1997; ccepted 6 My 1998) SUMMARY We exmined the roles tht sesonl shifts in precipittion nd temperture plyed in the ectomycorrhizl (ECM) coloniztion of pinyon pine (Pinus edulis Engelm.) t two contrsting sites in northern Arizon. Pinyons growing in sh nd cinder soils experienced much greter wter nd nutrient stress thn pinyons growing nerby in sndylom soils. Over one yer period, we obtined monthly mesurements of ECM coloniztion, root zone soil moisture nd temperture, nd ir temperture nd precipittion. Four mjor ptterns emerged. Firstly, lthough climte s mesured by mbient temperture nd precipittion did not vry between the two sites, soil temperture ws significntly higher nd soil moisture significntly lower t the cinder site thn t the sndy-lom site. Secondly, ECM coloniztion ws significntly higher t the cinder site for 5 of 12 months. Thirdly, lthough nerly 7% of the vrition in ECM coloniztion of pinyons growing in cinder soil ws predicted by combintion of soil moisture nd soil temperture, these sme vribles hd little predictive power for pinyons growing in sndy-lom soils. Air temperture nd precipittion were lso significntly correlted with ECM coloniztion t the cinder site but not the sndy-lom site. Fourthly, wtering experiment showed tht ECM coloniztion significntly incresed with supplementl wter t the cinder site, but not t the sndy-lom site. Thus, in two sites tht did not differ in plnt community or climte, ectomycorrhizs in cinder soils were fr more sensitive to chnges in moisture nd temperture thn ectomycorrhizs in sndy-lom soils. Key words: Ectomycorrhizl fungi, ectomycorrhizl coloniztion, temporl vrition, environmentl stress, cinder-sh soils. INTRODUCTION The extent of root coloniztion by ECM fungi cn be influenced by fetures of the host plnt, such s root physiology nd morphology (Wilcox, 1968), by mycorrhizl fungl hyphl structure nd phenology (Brundrett, 1991), nd by soil conditions nd climtic fctors (Brundrett, 1991; Bowen, 1994). Soil moisture nd soil temperture cn hve significnt effects on ectomycorrhizl coloniztion (Hcskylo, Plmer & Vozzo, 1965; Hrvey, Jurgensen & Lrsen, 1978; Prke, Lindermn & Trppe, 1983; Ingleby, Lst & Mson, 1985; Smson & Fortin, 1986; Rstin et l., 199; Blsius, Kotte & Oberwinkler, 1989) nd this sensitivity of ectomycorrhiz to chnges in temperture nd soil moisture could led to significnt sesonl vrition in coloniztion. However, few studies hve exmined sesonl vrition in ECM coloniztion, * To whom correspondence should be ddressed. E-mil: rls6 dn.ucc.nu.edu nd the results of these studies hve been mixed. Sesonl vrition in ECM coloniztion hs been reported in studies of spruce (Abies spp.) stnd in Polnd (Twrowski, 1963), Dougls fir nd lrch stnd (Pseudotsug menziesii nd Lrix spp.) in Montn (Hrvey et l., 1978), two Pcific silver fir (Abies mbilis) stnds in Oregon (Vogt et l., 198) nd Norwy spruce stnd (Pice bies) in Germny (Blsius et l., 1989). No significnt sesonl vrition in mycorrhizl inoculum levels ws reported in jrrh forest in Austrli (Brundrett & Abbott, 1994) or in totl ECM frgments in Dougls-fir stnd in western Oregon (Fogel & Hunt, 1979). Most studies exmining temporl vrition in ECM coloniztion hve been conducted only during the growing seson, or hve smpled ECM popultions infrequently. In this study we mesured ECM coloniztion of pinyon pines (Pinus edulis Engelm.) long with soil moisture, soil temperture, mbient temperture nd precipittion for 1 yr t two field sites differing in soil type. The two sites

2 734 R. L. Swty nd others Tble 1. A comprison of the cinder nd the sndy-lom site Prmeter Cinder site Sndy-lom site Men mbient temperture ( C) Men dily precipittion (mm) Soil moisture (% wter)* Soil temperture ( C)* Extrctble phosphte (µg g soil)b* Soil NO minerliztion (µg g soil d )b* Soil NH minerliztion (µg g soil d )b* Cone production (men no. femle 185 cones per tree per site)c* Wter stress (xylem pressure; MP)d* Growth (stem length in mm)e* Dt from current study; dily mbient temperture nd precipittion obtined from Ntionl Prk Service. b Adpted from Gehring & Whithm (1994). c Men number of totl conelet production per tree in 1988 bsed on minimum of nine trees per site (extrpolted from Christensen & Whithm (1991): Fig. 1). d Men wter stress for pinyons growing in one cinder nd one sndy-lom site (extrpolted from Mopper et l. (1991): Fig. 2). e Men stem length dt over n 11-yer period from one cinder site nd one sndy-lom site, (Cobb, unpublished). * Comprisons significnt t P 5. were similr in elevtion, men nnul precipittion nd men nnul temperture, but one site hd sh nd cinder soils low in nutrients nd moisture wheres the other site hd sndy lom soils significntly higher in nutrients nd moisture (Christensen & Whithm, 1991; Mopper et l., 1991; Gehring & Whithm, 1994, 1995; Cobb et l., 1997) (Tble 1). Plnt performnce prmeters such s wter stress nd shoot growth were lower in pinyons growing in cinder soils thn pinyons growing in sndy-lom soils (Tble 1). Ectomycorrhizl coloniztion lso vried between these two environments t one period of the yer (Gehring & Whithm, 1994, 1995), but responses of ectomycorrhiz to temporl vrition in soil moisture nd soil temperture were not ddressed. By utilizing this system, in which edphic fctors vried significntly but climte ws similr, we hoped to understnd better the role of soil fctors in influencing chnges in ECM coloniztion through time. We ddressed the following questions: (1) does ECM coloniztion chnge significntly over time t either the cinder site or the sndy-lom site nd re there differences between the sites in the mgnitude of this chnge?; (2) do temporl chnges in ECM coloniztion correlte with soil moisture nd or soil temperture chnges nd re the responses similr in the two environments?; (3) re soil prmeters, mesured t the time of collection better predictors of ECM coloniztion thn monthly mens of ir temperture nd rinfll collected t nerby wether sttion?; (4) Cn we lter ECM coloniztion by mnipulting soil wter? MATERIALS AND METHODS Study site descriptions The cinder soil site we studied ws locted south of Sunset Crter Ntionl Monument, Coconino County, AZ, USA (elevtion 1859 m). The soils t this site were composed of sh, lv nd cinders (Hendricks, 1985). The sndy-lom study site ws 22 km wy ner Wlnut Cnyon Ntionl Monument, Coconino County, AZ, USA (elevtion 195 m) nd ws mde up of sndstone nd limestone-derived soils (Hendricks, 1985). Plnt communities t both sites were dominted by pinyon pine (P. edulis), one-seed juniper (Juniperus monosperm Engelm.) nd ponderos pine (Pinus ponderos Lwson). Grsses were rre t the cinder site, nd Gmbel s (Quercus gmbellii Nutt.) ok ws bsent. At the sndy-lom site, grsses were more common nd there were few clones of Gmbel s ok. The ECM tree species present t one or both sites were pinyon pine, ponderos pine, nd Gmbel s ok. Ectomycorrhizl coloniztion Monthly, from September 1995 to August 1996, root smples were tken from 25 previously unsmpled, mture trees (i.e. those tht produced femle cones) with trunk dimeters cm t 2 cm boveground t ech study site. Roots were sorted from soil smples obtined with shovel from inside the cnopy, on the west side of ech tree t depth of

3 Temporl vrition in ectomycorrhizl coloniztion 735 Tble 2. Results of two-wy ANOVA of dt from the cinder nd the sndy-lom site Site (d.f. 1) Time (d.f. 11) Interction (d.f. 11) Prmeter F P F P F P Air temperture Precipittion Soil temperture Soil moisture Ectomycorrhizl coloniztion cm. The mjority of pinyon fine roots occurred in the top 2 cm of the soil t both sites. An verge of 85 short roots were scored from ech tree t ech time. Gehring (unpublished) hs found tht scoring 8 root tips per tree provided similr estimtes of ECM coloniztion to scoring 3 5 times tht number. The techniques of Gehring & Whithm (1991) were used to distinguish ECM from non- ECM nd living from non-living roots. Percentge ECM coloniztion ws clculted s the number of ctive ECM root tips divided by the totl number of short roots (Gehring & Whithm, 1994). To determine if there were site differences nd or temporl vrition in ECM coloniztion, we used two-wy ANOVA with time nd site s tretment fctors. We used Levene s test to determine if the degree of temporl vrition differed between the sites. These nd ll subsequent sttisticl nlyses were performed using SPSS for Windows, relese 6. Soil nd climte prmeters We mde monthly mesurements of soil moisture nd soil temperture to determine whether ECM coloniztion ws predicted by environmentl prmeters. In the cvity dug to obtin root smples of ech smple tree, soil temperture ws mesured with VSR soil thermometer tht ws positioned next to the roots tht were smpled for nlysis of ECM coloniztion. Approximtely ml of soil ws collected from this sme cvity ner the roots nd stored in plstic bgs until grvimetric soil nlysis ws performed. Dily ir temperture nd precipittion mesurements were obtined from the Visitor Centers t Sunset Crter nd Wlnut Cnyon Ntionl Monuments (ech within km of the study sites). Multiple regression nlysis ws used to exmine the reltionships between ECM coloniztion nd environmentl prmeters. Wtering experiment In order to test experimentlly the hypothesis tht dditionl wter ffected ECM coloniztion, five control pinyons were pired for size nd loction with five tretment pinyons t ech site. The control nd tretment trees hd trunk dimeters rnging from to 15 cm t 2 cm from the ground nd were given gllons of wter every 4 d for three weeks t ech site. Becuse of the drought conditions of the summer of 1996, the wtering experiment ws conducted in erly July, when monsoonl rinfll ws significntly less thn norml. Three weeks fter the wtering tretment begn, soil moisture, nd ECM coloniztion were mesured t ech tree s described bove. Pired t-tests were used to compre ECM coloniztion nd soil moisture between wtered nd control trees. RESULTS Climte dt We found no significnt differences in mbient ir temperture between the cinder nd sndy-lom sites but did find significnt chnges in mbient temperture over time (Tble 2, Fig. 1 ). There were no significnt site time interctions. The men dily mbient temperture t the cinder soil site ws 2 3 C, with minimum temperture of 3 3 C nd mximum temperture of 36 7 C. The men dily mbient temperture t the sndylom site ws 2 8 C with minimum temperture of 17 8 C nd mximum temperture of 37 2 C. We lso found no significnt differences in precipittion between the sites lthough rtes of precipittion chnged significntly over time t both sites (Tble 2, Fig. 1b). There ws no site time interction. The totl nnul precipittion t the cinder site ws 59 7 cm wheres the totl precipittion for the sndy-lom site ws 59 5 cm. For both sites, the periods with the highest levels of precipittion occurred during the winter months nd during the lte summer nd erly utumn. Soil prmeters Although the climtes t the two sites were similr, we found significnt differences in the temperture of the soil t the two sites. Soil temperture chnged significntly over time nd there ws significnt site time interction indicting tht the soil temperture differences between the two sites vried with time (Tble 2, Fig. 2). Sttisticl nlysis of

4 736 R. L. Swty nd others 35 () () Averge dily temperture ( C) Soil temperture ( C) S O N D J F M A M J J A 5 12 (b) Averge dily precipittion (cm) (b) S O N D J F M A MJ J A Month Figure 1. Men dily mbient temperture () nd precipittion (b) dt obtined from Sunset Crter Ntionl Monument (, cinder site) nd Wlnut Cnyon Ntionl Monument (, sndy-lom site) from September, 1995 to August, 1996 (men 1 SE). ech month individully indicted tht soil temperture differed significntly between the sites during ll months of the yer, with the cinder site hving the higher vlue in nine of the 12 months (Fig. 2). The men soil tempertures were 17 2 C for the cinder soil nd 13 8 C for the sndy-lom soil. The two sites lso differed significntly in soil moisture which chnged significntly over time. Agin there ws significnt site time interction, indicting tht soil moisture responses with time vried between the sites (Tble 2, Fig. 2 b). Sttisticl nlysis of ech month seprtely showed tht soil moisture ws significntly lower out of 12 months t the cinder soil sites, with the two exceptions occurring when the smple dte immeditely followed period of rin. The nnul men grvimetric soil moisture ws 3 3% for the cinder soil site nd 5 6% for the sndy-lom site. % Soil moisture % Ectomycorrhizl coloniztion S O N DJ F MAMJ J A (c) S O N D J F M A M J J A Month Figure 2. Temporl vrition in soil temperture (), % soil moisture (b), nd % ectomycorrhizl coloniztion (c) for September, 1995 through August, 1996 (men 1 SE). All vlues were obtined from the root zone t the cinder ( ) nd the sndy-lom ( ) sites. Temporl vrition in ectomycorrhizl coloniztion Both soil type nd month of smpling hd significnt effect on ectomycorrhizl coloniztion (Tble 2, Fig. 2 c). There ws lso significnt time site interction, indicting tht the reltionships between the sites chnged with time. Seprte nlyses for ech month indicted tht ECM coloniztion ws significntly higher t the cinder site thn the sndy-lom site during 5 months of the yer (Sept., Oct., Mr., July nd Aug.). Further-

5 Temporl vrition in ectomycorrhizl coloniztion 737 more, the mgnitude of the chnge in ectomycorrhizl coloniztion with time ws significntly greter (4 times) t the cinder site thn t the sndylom site (t 2 35, d.f. 11, P 38). Ectomycorrhizl coloniztion rnged from 35 3 to74 1% (38 8% difference) t the cinder site nd from 35 1to 44 4%, (9 3% difference) t the sndy-lom site. Reltionship between ectomycorrhizl coloniztion nd soil nd ir prmeters A multiple regression nlysis demonstrted tht soil moisture nd soil temperture combined significntly correlted with ECM coloniztion t the cinder site (r 675, F 381, P 4). Prtil regression results indicted tht soil moisture nd soil temperture both hd significnt effect on ECM coloniztion t the cinder site (β 647, t 3 45, P 6 for soil moisture nd β 715, t 3 812, P 3 for soil temperture). This result contrsted with the pttern t the sndy-lom site, where soil moisture nd soil temperture did not hve significnt effect on ECM coloniztion (r 8, F 1 94, P 336). Similrly, combintion of men mbient temperture nd men precipittion for the month before smpling ws n excellent predictor of ectomycorrhizl coloniztion t the cinder site (r 941, F 38 75, P 1). Both precipittion nd temperture contributed significntly to the regression (β 74, t 6 42, P 1 for precipittion, β 392, t 3 391, P 1 for temperture). Agin, trees t the sndy-lom site showed different pttern, with no significnt reltionship between mbient temperture combined with precipittion nd ECM coloniztion (r 97, F 324, P 735). At the cinder site, the combintion of mbient temperture nd men monthly precipittion gve higher regression vlues for ECM coloniztion thn the combintion of soil temperture nd soil moisture. Ectomycorrhizl responses to dded wter Bsed on our observtion tht soil moisture ffected ECM coloniztion (Fig. 1 ) we predicted tht dding wter would hve significnt effect on ECM coloniztion t the cinder site, but no impct on ECM coloniztion t the sndy-lom site. Wtering significntly incresed soil moisture t both sites (cinder, t 5 39, P 3; sndy-lom, t 3, P 14) (Fig. 3). We found significnt differences in ECM coloniztion between the wtered nd control trees t the cinder site (t 3 8, P 2), where wtered trees hd 19 2% higher levels of ECM coloniztion thn controls. However, there were no significnt differences in ECM coloniztion between wtered nd control trees t the sndy-lom % Soil moisture % Ectomycorrhizl coloniztion b b Cinder site Sndy-lom site Figure 3. Men percentge soil moisture () nd men percentge ectomycorrhizl coloniztion (b) for wtered ( ) nd control ( ) groups t the cinder nd sndy-lom sites. Different letters bove histogrms indicte significnt differences (P 5). Brs represent mens 1 SE. site (t 1 62, P 9) (Fig. 3b). Therefore, in both observtionl nd experimentl studies, we found tht ECM coloniztion ws more responsive to chnges in environmentl prmeters t the cinder soil site thn t the sndy-lom site. DISCUSSION Vrible responsiveness of ectomycorrhizl coloniztion to soil nd climte prmeters Although the cinder nd sndy-lom sites studied here experienced the sme climte, we observed three mjor differences in ECM coloniztion between pinyons growing in the two sites. First, ECM coloniztion ws significntly higher t the cinder site thn the sndy-lom site during 5 months of the yer. This corrobortes previous findings tht were limited to spring nd fll smpling (Gehring & Whithm, 1994, 1995). Second, the temporl vrition in ECM coloniztion ws 4 times greter t the cinder site thn t the sndy-lom site. Third, the degree of responsiveness to environmentl prmeters differed between the two sites, with ECM coloniztion t the cinder site vrying significntly with climte nd soil prmeters wheres no b

6 738 R. L. Swty nd others significnt reltionship between the sme prmeters ws observed t the sndy-lom site. The difference in responsiveness ws lso observed following supplementl wtering which resulted in chnges in ECM coloniztion t the cinder site but not t the sndy-lom site. Fluctutions in ECM coloniztion with sesonl fluctutions in temperture nd moisture could be dvntgeous to plnts, prticulrly those growing in nutrient-poor soils or drought situtions. Ectomycorrhiz hve been hypothesized to be most importnt in soils where the need for enhnced nutrient nd wter uptke is the gretest (Meyer, 1973), nd incresed numbers of ECM roots during moist times might llow plnts to mximize wter nd nutrient uptke. Furthermore, in rid environments, photosynthetic rtes cn be suppressed during dry times of the yer (Ljth & Getz, 1993), potentilly reducing the bility of plnts to support ECM fungl mutulists. Giovninni et l. (unpublished) hve shown tht the photosynthetic rtes of pinyons growing in cinder soils re highly sensitive to moisture with peks in photosynthetic ctivity occurring in the spring nd following the summer monsoon rins. These dt suggest tht incresed photosynthetic rtes could coincide with incresed ECM coloniztion in pinyons t the cinder site. Perhps more surprising ws the lck of effect of vrition in ir or soil temperture or moisture on ECM coloniztion t the sndy-lom site. Severl reserchers hve found significnt reltionships between ir nd or soil climte nd ECM coloniztion (Hrvey et l., 1978; Vogt et l., 198; Blsius et l., 1989; Rstin et l., 199; Antibus & Linkins, 1992). For exmple, sesonl vrition in Dougls fir nd lrch ECM root tip counts in western Montn were prtly ttributed to chnges in soil temperture nd soil moisture (Hrvey et l., 1978). Additionlly, temporl vrition in number of living ectomycorrhiz of Norwy spruce trees in Germny ws reported in two studies (Blsius et l., 1989; Rstin et l., 199). By contrst, in biossy experiments, no temporl vrition or correltion between climte nd ECM fungl inoculum levels ws found in jrrh forest of Austrli (Brundrett & Abbott, 1994). Although we expected tht soil prmeters would hve the highest correltion with ECM coloniztion, the best predictor of ECM coloniztion t Sunset Crter proved to be combintion of mbient temperture nd precipittion. We hypothesize tht this pprent contrdiction ws due to the smpling methods employed. The soil prmeters were mesured once per month on the dy of ECM smpling wheres mbient temperture nd precipittion vlues were monthly mens of dily mesurements. The soil vlues might not hve been n ccurte representtion of the rnge of conditions experienced by the ECM roots between smpling periods. For exmple, in Mrch, 1996, soil moisture ws times greter (11% compred with 1%) thn the previous month. This bnormlly high reding ws due to rinfll the dy before smpling. However, men monthly precipittion for Februry nd Mrch vried only twofold, 5 mm in Februry nd 25 mm in Mrch. More frequent soil smpling would probbly hve improved the reltionship between soil prmeters nd ECM coloniztion t the cinder site. Implictions Ectomycorrhizl coloniztion vried with time t both cinder nd sndy-lom sites, but to mrkedly different degree t the two sites. Our dt were consistent with the hypothesis tht ectomycorrhiz t one site responded to environmentl chnges differently thn t the other site. We were surprised to observe such different ptterns of response in the sme plnt species growing in two res of nerly identicl climte. Our findings rgue for more studies on the dynmics of ECM ssocitions through time in vriety of environments. One of the potentil resons for the differences we observed between the sites is tht the community of ECM fungl ssocites of pinyon pines t cinder nd sndy-lom sites cn differ mrkedly (Gehring et l., 1997). These community differences might hve contributed to the differentil responses to climte we observed t the two sites. The dt of Gehring et l. (1997) combined with our results rgue for further reserch on the functionl ttributes of different fungl species under vriety of environmentl conditions. ACKNOWLEDGEMENTS We thnk the United Sttes Forest Service for their coopertion, K. Ogle, R. St. Lurent nd N. Cobb for sttisticl nd computer dvice, nd G. Wimp, J. White nd two nonymous reviewers for commenting on the mnuscript. This reserch ws supported by DOE grnt DE-FG3-94ER61849, USDA grnt nd NSF grnt DEB REFERENCES Antibus RK, Linkins AE III Effects of liming Red Pine forest floor on mycorrhizl numbers nd mycorrhizl nd soil cid phosphtse ctivities. 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