Growth and root system development of white oak and loblolly pine as affected by simulated acidic precipitation and ectomycorrhizal inoculation

Forest Ecology and Management, 46 ( 1991 ) 123-133

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Elsevier Science Publishers B.V., Amsterdam

Growth and root system development of white oak and lobiolly pine as affected by simulated acidic precipitation and ectomycorrhizal inoculation* R.F. Walker ~ and S.B. McLaughlin b ~University of Nevada, Reno. Department of Range, Wildhfe, and Forestry, 1000 Valley Road, Reno. NV8951Z USA bOak Ridge National Laboratory. Environmental Sciences Division. Building 1505. Oak Ridge. TN 37831, USA (Accepted 17 October 1990 )

ABSTRACT Walker, R.F. and McLaughlin, S.B., 1991. Growth and root system development of white oak and Ioblolly pine as affected by simulated acidic precipitation and ectomycorrhizal inoculation. For. Ecol. Manage., 46: 123-133. Individual and interactive effects of simulated acidic rainfall and ectomycorrhizal inoculation on growth of white oak ( Quercus alba L. ) and Ioblolly pine (Pinus taeda L. ) were examined. Seedlings of each species inoculated with basidiospores of Pisolithus tinctori,ls (Pers.) Coker and Couch and uninoculated control seedlings were exposed to two simulated rains per week ofpH 4.8, 4.2 or 3.6, for 26 weeks. After the exposures, mycorrhizal quantification of complete root systems revealed that ectomycorrhizal development, whether by P. tinctorius on inoculated seedlings or by naturally occurring fungi on control seedlings, was greater on loblolly pine than on white oak. Also, although ectomycorrhizal development was greatest on loblolly pine treated with the most acidic of the simulated rains, there was no consistent effect of increasing acidity on mycorrhizal development of white oak. Diameter growth of white oak and height and diameter growth of lohloily pine were significantly increased by'the P. ti.nctoriusinfection. Within both mycorrhizal treatments, exposure to rains ofpH 3.6 significantly reduced the diameter growth of white oak, but rainfall acidity had little effect on the growth of Ioblolly pine. Of the variables examined, the data presented here suggest the primary effect of acid precipitation on white oak seedlings is on shoot diameter, whereas its primary effect on Ioblolly pine seedlings is on mycorrhizal development.

INTRODUCTION

Interest in potential effects o f acidic deposition on forest trees encompasses both direct effects on exposed plant surfaces as well as indirect effects result*Publication No. 3212, Environmental Sciences Division, ORNL.

© 1991 Elsevier Science Publishers B.V. All rights reserved 0378-1127/92/$03.50

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R.F, WALKER AND S.B, McLAUGHLIN

ing from altered soil chemistry. Four principal mechanisms of logical concern have been emphasized with respect to impacts of acid rain on forest growth: ( 1 ) altered plant water relations, (2) altered forest nutrition, (3) direct effects on growth and growth processes, and (4) indirect effects on resistance to biotic stresses (McLaughlin, 1984). Many mechanism~ of interaction with implications of a potential reduction in tree growth can be hypothesized based on known relationships between soil-plant systems and acidity. However, no documented studies have demonstrated in forest tree seedlings a negative growth response solely attributable to rain of ambient or near-ambient acidities. Nevertheless, declining growth rates in recent years of spruce and fir in mid-Appalachian USA subalpine forests (Adams et al., 1985 ) and of pine in the Piedmont region forests of the southeastern USA (Sheffield and Knight, 1984; Tansey, 1984) indicate that forest decline is not restricted solely to the Northeast. Furthermore, because any explanation for this growth decline is largely speculative at present (Lucier, 1988 ), studies concerned with all potential causal factors, including precipitation of ambient acidity, at all stages of tree growth are warranted. Mycorrhizal symbioses are of indisputable importance to forest trees. Most conifers are obligately ectomycorrhizal (Meyer, 1973 ), a consideration which has prompted efforts to develop and perfect methods for inoculating pines with specific ectomycorrhizal symbionts (Marx et al., 1984). However, Ulrich et al. (1980) in Germany presented evidence of the toxicity of an increased soil Al concentration to fine roots of European beech (Fagus sylvatica L.). The increased concentrations were attributed to the mobilization of Al resulting from natural and anthropogenic soil acidification. The implications of these findings for mycorrhizal associations, and thus growth, of forest trees are obvious and form a partial basis for current concerns over long-term effects of acidic rain on regional forest productivity. The study reported here concerns the effects of factorial combinations of simulated rains of ambient and near-ambient acidities and ectomycorrhizal inoculation with basidiospores of Pisolithus tinctorius (Pets.) Coker and Couch on the growth and root system development of white oak (Quercus alba L.) and loblolly pine (Pinus taeda L.) seedlings. This study is one of a series currently being done to examine the interactions of acidic rain, ozone, substrate fertility, and mycorrhizal inoculation on growth and root system development, water relations, and uptake of essential nutrients and potentially toxic metallic elements of seedlings of these two commercially important species. MATERIALS AND METHODS

White oak acorns (Madison County, TN, seed source) were sterilized by soaking in 5% H202 for 10 min followed by rinsing in tap water for an addi-

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tional 10 min. After sterilization, a germination test revealed the germination success of the acorns to be approximately 50%. Loblolly pine seeds (Lincoln County, GA, seed source) were soaked in tap water for 24 h and then stratified for 6 weeks at 3°C. The seeds were then sterilized by soaking in 10% H202 for 30 rain, and then rinsed in tap water for an additional 10 min. A subsequent germination test revealed the germination success of the loblolly pine seed to be approximately 67%. The potting medium consisted of a Sensabaugh loam collected from an old field site on the US Department of Energy Oak Ridge Reservation (Roane County, TN). The soil was taken from the upper 30 cm of the profile, fumigated for 96 h with a methyl bromide-chloropicrin formulation (Dowfume MC-2, Dow Chemical Co., Midland, MI) using 890 g fumigant m -3 of soil, aerated for 12 days, and then mechanically shredded and mixed. After soil preparation, each of 48 7.6-1 greenhouse pots were filled with approximately 7.7 kg of soil. For white oak, each pot was then sown with 12 acorns divided equally among three equidistant groups; for loblolly pine, each pot was sown with nine seeds divided equally among three equidistant groups. After germination, the seedlings of both species were thinned to three equidistant plants per pot. The pelletized basidiospore inoculum ofP. tinctorius used in this st:~dywas produced by the International Forest Seed Company (Odenville, AL) and consisted of spores attached to vermiculite particles by a water-soluble adhesive. Each pellet contained approximately 3 × 106 spores. Vermiculite particles coated with adhesive but without spores were used in the production of uninoculated control seedlings. Seven weeks after planting, appropriate seedlings of each species were inoculated with P. tinctorius by applying 12 spore pellets to each seedling at the soil surface followed by light irrigation with distilled water to dislodge the spores from the vermiculite particles. The inoculation procedure was repeated 14 weeks after planting and again after 21 weeks. Pellets without spores were applied to control seedlings of each species in a manner and on a schedule identical to that used for inoculated seedlings. The seedlings were exposed to simulated rains ofpH 4.8, 4.2 or 3.6 via the system described by Shriner (1979), which provided rain droplets in an approximate 2 m fall to plants on a rotating platform. Stock solutions containing sulfuric and nitric acids, plus appropriate trace elements as noted by Irving ( 1985 ), were added to a distilled water stream by way of metering pumps such that the final concentration of ions was similar to those found in natural rainwater. Rain solutions were dispensed through nozzles which distributed the droplets evenly over the platform. During each exposure, all seedlings received a measured 1.2 cm of rain of appropriate pH, which was monitored periodically throughout the exposure. All seedlings were subjected to two exposures per week for a total of 26 weeks beginning at sowing. Total rainfall received by seedlings in this study approximated the 35-year mean of precip-

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itation during the growing season (April-September) on the Oak Ridge Reservation (S.D. Swisher, Atmospheric Turbulence and Diffusion Laborator,, Oak Ridge, TN, personal communication, 1985). Between exposures~ the seedlings were placed in a fiberglass greenhouse. Supplementary lighting was not required because the experiment was initiated and completed during the normal growing season. Maximum day temperatures averaged 34°C (range 20-38 ° C ) and minimum night temperatures averaged 19 ° C (range 9-24 ° C ). Measurements of height (cm) and stem diameter ( m m ) at the soil line were made 13 and 26 weeks after sowing. After the final measurements, shoots of all seedlings were harvested, dried at 100 °C for 48 h, and weighed (nearest 0.01 g). All root systems were harvested and washed, and their ectomycorrhizal development was quantified. This was accomplished by measuring the total length (cm) of all lateral roots of 1 cm length or more, counting the unit lengths (cm) of lateral roots bearing ectomycorrhizae as evidenced by bifurcate or coralloid short roots or short roots with an obvious fungal mantle, and expressing lateral root unit lengths with ectomycorrhizae as a percentage of the total length of the lateral roots for each root system. Records ofP. tinctorius ectomycorrhizae, which were identified by their characteristic appearance (Marx and Bryan, 1975 ), were kept separate from those of other fungi. After mycorrhizal quantification, the root systems were dried and weighed as described previously for shoots and shoot/root ratios were calculated. Each of the 12 factorial combinations of two species, two mycorrhizal treatments, and three rain treatments was replicated four times, with the three seedlings in each greenhouse pot constituting a replication. Data from each of the two species were analyzed separately as 3 × 2 factorial experiments. Analyses of variance were performed on all data and treatment effects were considered to be significant only when P_< 0.05 as indicated by F-tests. Differences among means were evaluated using Duncan's multiple range test with a=0.05. Before analysis, the arcsine transformation was peribrmed on all percentage data. All analyses were accomplished with the Statistical Analysis System (SAS Institute, Inc., Cary, NC). RESULTS

There was substantial development ofP. tinctorius ectomycorrhizae on roots of both white oak and loblolly pine in response to inoculation with spores of this symbiont, but these ectomycorrhizae were more prevalent on the pines than on oaks (Table 1 ). This symbiont comprised the total mycorrhizal formation of inoculated seedlings of both species. None of the control seedlings of either species were infected by P. tinctorius, and overall, mycorrhizal development of these seedlings was poor. It is likely that the few mycorrhizae on control seedlings of both white oak and loblolly pine resulted from windborne spores entering the greenhouse from nearby forest stands. Analyses of variance indicated that the total lateral root length of the white

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TABLE 1 Effects of factorial combinations of two mycorrhizal treatments and three simulated acid rain treatments on seedling development of white oak and loblclly pine I Mycorrhizal treatment

White oak

Loblolly pine

pH of simulated rain 4.8

4.2

Mean pH of simulated rain 3.6

4.8

Ectomycorrhizal infection attributable to P. tinctodus (%) Inoculated 19b 26a 24ab 23 41b Uninoculated Oc Oc Oc 0 Oc Mean 10 13 12 21 Ectomycorrhizal infection attributable to other fungi (%) Inoculated 0b 0b 0b 0 0c Uninoculated 0b 0b la 0 2b Mean 0 0 1 ! Total length of lateral roots (cm) Inoculated 573a 616a 687a 625 308ab Uninoculated 570a 749a 510a 610 26lab MeaI~ 572 683 599 283 Dry weight o[ shoots (g) Inoculated 1.34a 1.40a !.34a 1.36 2.25a Uninoculated 1.06ab 1.17ab 0.97b ! .07 0.37b Mean 1.20 1.29 1.16 1.31 Dry weight of roots (g) Inoculated 3.92a 4.05a 3.76ab 3.91 0.49a Uninoculated 2.72ab 3.02ab 2.49b 2.74 0.16b Mean 3.32 3.54 3.13 0.33 Shoot/root ratio Inoculated 0.44a 0.37a 0.38a 0.40 5.44ab Uninoculated 0.4D 9.52a 0.43a 0.45 2.68c Mean 0.43 0.45 0.41 4.06 Height after 13 weeks (cm) Inoculated 12.4a 12.9a 12.6a 12.6 13.0a Uninoculated 1i.Sa 13.0a 11.2a 11.9 10.9a Mean i 2.0 13~0 I 1.9 12.0 Stem diameter after 13 weeks (ram) Inoculated 3.6a 3.7a 3.2b 3.5 2.2a Uninoculated 3.0be 2.9bc 2.6c 2.8 l.ga Mean 3.3 3.3 2.9 2.1 Height after 26 weeks (cm) Inoculated 12.5a 13.1a 12.7a 12.8 26.9a Uninoculated I 1.6a 13.1a 11.3a 12.0 11.4b Mean 12.1 13.1 12.0 19.2 Stem diameter after 26 weeks (mm) Inoculated 3.9a 3.8a 3.2b 3.6 3.6a Uninoculated 3.2b 3.0be 2.7c 3.0 2.0b Mean 3.6 3.4 3.0 2.8

4.2

Mean 3.6

40b Oc 20

51a Oc 26

44 0

0c 2b !

0c 4a 2

0 3

360a 200b 280

219ab 195b 207

296 219

2.06a 0.35b 1.21

!.89a 0.39b 1.14

2.07 0.37

0.45a 0.13b 0.29

0.3lab 0.12b 0.22

0.42 0.14

5.02bc 3.08bc 4.05

7.57a 3.48bc 5.53

6.01 3.08

14.4a 10.3a 12.4

13.3a 11.3a 12.3

13.6 10.8

2.1a 1.9a 2.0

2.1a 1.Ta 1.9

2.1 1.8

26.3a 1l.Sb 18.9

25.5a 12.1b 18.8

26.2 11.7

3.4a 2.0b 2.7

3.3a 1.9b 2.6

3.4 2.0

1Within a species and measurement variable, means sharing a common letter do not differ significantly at c~= 0.05 according to Duncan's multiple range test.

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R.F. WALKER AND S.B. McLAUGHLIN

oak was not significantly affected by inoculation with P. tinctorius, but inoculation with this symbiont increased lateral root length of loblolly pine by 35%. Similarly, the shoot/root ratio of white oak was not affected by mycorrhizal treatment, but the shoot/root ratio of the loblolly pine with P. tinctorius ectomycorrhizae was 95% larger than that of uninoculated loblolly pine. St..opt and root dry weights of both white oak and loblolly pine, however, were significantly increased by the P. tinctorius infection, although the disparity between mycorrhizal treatments was far more pronounced in the latter species. In white oak, shool weight was increased 27% and root weight 43% in comparison with uninoculated seedlings, whereas in loblolly pine, shoot and root weights were 459% and 200% greater, respectively, in inoculated seedlings. Height and stem diameter growth were also more affected by inoculation with P. tinctorius in loblolly pine than in white oak. After both 13 and 26 weeks, the differences in height between mycorrhizal treatments were nonsignificant in the white oak, whereas stem diameter of inoculated white oak was 25% larger after 13 weeks and 20% larger after 26 weeks than that of uninoculated seedlings. In loblolly pine, however, height growth was increased 26% by the P. tinctorius infection after 13 weeks and 124% after 26 weeks, and diameter growth was increased 17% and 70% at the mid-study and final measurements, respectively. The degree of infection by P. tinctonTus was significantly higher in inoculated oaks exposed to simulated rains ofpH 4.2 than in those which received rains of pH 4.8, and although the infection of inoculated oaks exposed to pH 3.6 rains did not differ significantly from that for either of the other two rain treatments, it closely approximated the level for seedlings which received rains of the intermediate acidity. In the inoculated loblolly pine, the per cent infection by P. tinctorius of seedlings exposed to rains of oH 3.6 was significantly higher than those exhibited by seedlings exposed to rains of either of the other acidities. Furthermore, the degree of ectomycorrhizal infection in uninoeulated white oak and loblolly pine which received rains of the highest acidity also significantly exceeded that of seedlings exposed to less acidic rains, although mycorrhizal development of uninoculated seedlings of both species was poor overall. Grow~.h measurements of white oak revealed that stem diameter was the variable most affected by rain acidity for this species, and diameter growth was significantly reduced by exposure to rains ofpH 3.6 after both 13 and 26 weeks. At the final measurement, the mean diameter of inoculated oaks which had received rains ofpH 4.8 was 22% larger than that of inoculated seedlings exposed to rains of pH 3.6, and a similar comparison revealed a comparable disparity in diameter within uninoculated oaks. Total lateral root length, shoo~ and root dry weights, shoot/root ratio, and height growth of white oak, however, were not significantly affected by rain acidity, although the dry weights, shoot/root ratio, and height growth of seedlings exposed to the most acidic

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rains were generally less than those of seedlings which received rains of higher pH. Any definitive effects of rain acidity on shoot or root growth of lobloUy pine were not apparent in these data, and almost all growth differenceswithin mycorrhizal treatments were nonsignificant. The only exception was the shoot/root ratios of inoculated pines in which the ratio for seedlings exposed to rains ot pH 3.6 significantly exceeded that for seedlings which received pH 4.2 rains. Nevertheless, the loblolly pine also exhibited some evidence of a negaW,,e growth response to the high-acidity rains, as the total lateral root length, shoot and root dry weights, height growth after 26 weeks, and diameter growth after 13 and 26 weeks of seedlings which received rains of pH 3.6 were generally less than those of seedlings exposed to less acidic rains.

DISCUSSION

The fungus P. tinctorius has long been recognized as an ectomycorrhizal associate of both white oak and loblolly pine (Marx, 1977). In limited research, the inoculation of white oak with this symbiont has been shown to induce mycorrhizal development and subsequently to enhance the growth of this host (Marx, 1979), a finding further substantiated by the results pre= sented here. Comparatively, more research has been focused on the inoculation of loblolly pine with P. tinctorius (Marx and Bryan, 1975; Marx et al., 1976, 1984), and it has been demonstrated that these mycorrhizae stimulate the growth of this host on a wide variety of planting sites (Marx et al., 1977; Berry and Marx, 1978; Walker et al., 1989). Undoubtedly, the large growth differences between inoculated and uninoculated loblolly pine in this study were a function not only of the substantial formation of P. tinctorius mycorrhizae on inoculated seedlings but also of the sparsity of mycorrhizae on uninoculated seedlings, as a mycorrhizal infection is considered indispensable for the normal growth of pines (Meyer, 1973). In contrast, stimulation of white oak growth by the P. tinctorius infection was not as pronounced as that observed in loblolly pine. Cline and Reid (1982) observed that a minimal 40% P. tinctorius infection of P. contorta var. latifolia seedlings was required to achieve a substantial growth stimulation, and thus the disparate response of white oak and loblolly pine to inoculation reported here may largely reflect the differences in the degree of mycorrhizal development between the two species. These data also suggest that development of an ectomycorrhizal root system may be more vital for the normal growth of loblolly pine than for white oak. Mikola (1973), among others, has postulated that most ectomycorrhizal fungi are acidophilic. That this is the case for P. tinctorius, or at least that this

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R.E WALKER AND S.B. McLAUGHLIN

fungus readily adapts to acid environments, is well documented (Lampky and Peterson, 1963; Hile and Hennen, 1969; Marx, 1975; Walker, 1989). In this study, application of rains of pH 3.6 appeared to stimulate ectomycorrhizal development in both species, whether by P. tinctorius on inoculated seedlings or by naturally occurring fungi on uninoculated seedlings. The lone exception was found in inoculated white oak, where mycorrhizal development of seedlings exposed to rains ofpH 4.2 and 3.6 was similar. It is possible that the application of rains of the low, and perhaps the iptermediate, acidities depressed the pH of the growing medium and the mycorrhizae responded favorably to the increased acidity. These results contrast somewhat with those of Shafer et al. ( 1985 ) in which ectomycorrhizal formation by Thelephora terrestris (Ehrh.) Fr. and Laccaria laccata (Scop. ex Fr. ) Berk. and Br. on loblolly pine seedlings was inhibited by simulated rains of pH 4.0 and 3.2 in comparison with that which occurred on seedlings exposed to rains of pH 5.6 and 2.4. Also, Reich et al. ( 1985 ) found that ectomycorrhizal development in northern red ~ak (Q~.~orcusrubra L. ) seedlings was suppressed by application of simulated rains of pH 3.0 relative to that which occurred with application of less acidic rains, and Keane and Manning (1988) observed similar results in paper birch (Betula papyrifera Marsh.) seedlings exposed to simulated rains ofpH 3.5. Discrepancies between findings of the three studies cited above and the results presented here may be attributable to differences in overall experimental methods, host and symbiont species, and/or growing substrates, but nonetheless point to a need for further research before any generalization can be made on the impacts of acid deposition on ectomycorrhizal development. The most obvious conclusion that can be drawn from numerous studies that have been concerned with effects of acid precipitation on tree seedlings is that growth responses to varying levels of acidity differ markedly among species (Matziris and Nakos, 1977; Wood and Bormann, 1977; Lee and Weber, 1979; Raynal et al., 1982; Chappelka and Chevone, 1986). The data presented here indicate that exposure to rains of pH 3.6 suppressed the diameter growth of white oak seedlings in comparison with that exhibited by seedlings exposed to less acidic rains. The possible mechanisms by which this occurred include a reduced availability and/or uptake of essential nutrients, increased availability and uptake of potentially toxic metallic elements, and foliar injury with subsequent reduction in photosynthesis. The last was least likely to be a major factor, however, as within mycorrhizal treatments, foliar chlorosis and necrosis were observed to be generally less pronounced on seedlings which received rains of pH 3.6 than on those which received rains of pH 4.2, although both of these seedling groups appeared to have more diseased foliage than was observed on seedlings exposed to rains of pH 4.8. The marginally decreased growth of the loblolly pine which received the most acidic

GROWTH AND ROOT DEVELOPMENT OF WHITE OAK AND LOBLOLLY PINE

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rains can only be considered circumspect at present due to the exceedingly small differences between rain treatments within both mycorrhizal treatments. Rainwater o f p H 4.8 falls within the range o f acidities considered pristine by Charlson and Rodhe (1982). Rains o f p H 4.2 closely approximate a typical annual mean as monitored at the Walker Branch Watershed o f t h e rainfall on the Oak Ridge Reservation (Richter et al., 1983), and those o f p H 3.6 are within the range now c o m m o n l y encountered in the northeastern USA (Evans, 1982). Thus, the range o f p H values used here did not include unrealistic extremes in rainwater acidity. Nevertheless, the use o f sterilized potting soil and pure culture mycorrhizal inoculation in this study contribute to the inherent uncertainty o f extrapolating effects in the field from laboratory exI~riments and necessitate caution in drawing conclusions from these results concerning effects o f acid precipitation on the growth and mycorrhizal development o f forest tree seedlings. ACKNOWLEDGMENTS This research was sponsored by the US Environmental Protection Agency under Interagency Agreement 79-D-X0533 and the Office o f Health and Environmental Research, US D e p a r t m e n t o f Energy, under Contract No. DEAC05-840R21400 with Martin Marietta Energy Systems Inc.

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Tansey, J.B., 1984. The pine resource in South Carolina: an interim assessment, 1983. US Dep. Agric. For. Serv., Southeast. For. Exp. Sta. Res. Pap. SE-244, Asheville, NC, 22 pp. Ulrich, '.3., Mayer, R. and Khanna, P.K., 1980. Chemical changes due to acid precipitation in a loess-derived soil in central Europe. Soil Sci., 130:193-199. Walker, R.F., 1989. Pisolithus tinctorius, a Gasteromycete, associated with Jeffrey and Sierra lodgepole pines on acid mine spoils in the Sierra Nevada. Great Basin Nat., 49:1 ! 1-112. Walker, R.F., West, D.C., McLaughlin, S.B. and Amundsen, C.C., 1989. Growth, xylem pressure potential, and nutrient absorption of loblolly pine on a reclaimed surface mine as affected by an induced Pisolithus tinctorius infection. For. Sci., 35: 569-581. Wood, T. and Bormann, F.H., 1977. Short-term effects of a simulated acid rain upon the growth and nutrient relations ofPinus strobus, L. Water Air Soil Pollut., 7: 479-488.