I’ores~;;ology Management Forest Ecology andManagement83 (1996) 181-187
Variation in stable carbon isotope discrimination among and within exotic conifer species grown in eastern Nebraska, USA J.W. Zhang ap* , B.M. Cregg by1 * Department b USDA Forest
of Forestry, Service,
Fisheries and Wildlife, University of Nebraska at Lincoln, East Campus-UNL, Lincoln, NE 68583-0822, USA Rocky Mountain forest and Range Experiment Station, National Agroforestry Center, East Campus-UNL. Lincoln, NE 68583-0822, (I.54
Accepted 8 January19%
Abstract The study involved the measurement of stable-carbon isotopediscriminationandspecificleaf areaon foliageof mature treesof 11conifer speciesgrown in a common-garden in easternNebraska,USA. Eachspecieswasrepresented by threeto six treesfrom at leastthree populations.Carbonisotopediscriminationdiffered significantly amongspecies(F - 31.41, P < 0.0001)and amongpopulationswithin species(F - 1.65, P < 0.035). Of the all species,membersof the Pimceae family ( Abies, Larix, Picea, Pinus, Pseudorsuga) had muchhigher discrimination(A = 18.87,SE- 0.08, n = 141) than speciesin the Cupressaceae family (Juniperus) (A = 16.26,SE- 0.12, n - 18). A deciduousconifer, La-ix (A = 19.09, SE= 0.20, n = 16),did not differ significantlyfrom evergreenmembersof the Pinmeue family. Althoughspecificleaf area differed amongspecies(F = 152.62,P < 0.0001),it was not correlatedwith discrimination(r = 0.24, P > 0.14). Annual heightgrowth, specificleaf area,and annualprecipitationof seedsourceswereintercorrelated(0.605 r s 0.67, P < 0.01). No correlationwassignificantbetweenA andtheprecipitationor evapotranspiration of the seedsources.The resultsindicate that thesespecieshave different geneticstructuresandacclimationprocesses. Selectingfor better adaptedgenotypesbased on carbonisotopediscriminationmustbe speciesspecific. Keywords:
The Great Plains; Temperate
conifers;
Pinaceae;
Cupressaceae;
1. Introduction
For the last several decades, the USDA Forest Service and the University of Nebraska at Lincoln have established many plantations for species, provenance, and progeny testing in the Great Plains. The main objective of these plantations was to identify * Corresponding author. Tel.: (402) 437-5178; fax: 402-4375712; e-mail:
[email protected]. ’ Present address: Union Camp Corp., 1720 Goza Road, Mayesville, SC 29104, USA. 0378- 1127/%/$15.00 Copyright PII SO3781127(96)03723-
0 1996 Elsevier 1
Science
Provenance
test; Water-use
efficiency
the adapted species, provenances, or families for windbreaks, Christmas trees, and environmental and esthetic plantings in the region (Van Haverbeke, 1986a). The primary traits of interest were height and diameter growth. Physiological traits were largely ignored due to lack of instruments. Because physiological processes mediate genetic potential and environmental factors (Kramer, 1986), they may give a better indication of adaptedness of species or provenancesto the current or future environments.
In the past, plant scientists regarded instantaneous measure of photosynthetic rate as an explanation of
B.V. All rights reserved.
182
J.W. Zhang,
Table 1 Geographic species
information
and evapotranspiration.
Species
Provenance
Pinus strobus
L.
Pinus strobiformis
Pinus resinosa
Pinus nigru
Engelm.
Ait.
Arnold
Pinus sylvestris
L.
firms ponderosa Dougl. ex Laws.
Pinus banksiana
Lamb.
Pseudotsuga menziesii var. glauca (Beissn.) France
Picea pungens
Engelm.
L5ri.x leptolepis (Sieb. et Zucc.) Gotd
Juniperus
B.M. G-egg/Forest
virginiana
L.
annual height
Ecology
and Management
growth,
survival,
Latitude/Longitude
Elevation (ml
83 f 1996) I81-
and modelled ET (cm year-
water-use
’1
187
efficiency
AHG (cm year-
‘)
of provenances Survival (%) 75(4’
Mode&d WUE ‘--
Burke, NC Monroe, TN Fannin and Union GA
35”51’N/81°51’W 35”20’ i/84’ 10’ W 34°40’N/84010’W
450 550 600
68.55 15.77 81.05
64.O1”5’ 65.84 66.45
Taos, NM Mt. Lemmon, AZ Longvalley, AZ Yuma, MI St. Philomene, Quebec
36”20’N/ 105”4O’W 32”26’N/110”46’ W 38’26’N/ll lo1 1’W 44”30’N/86wO w 46’06’N/73”18’W
2130 2438 2255 305 19
57.23 64.38 65.39 59.58 58.72
30.14’9’ 24.42 26.08 49.38” ” 52.43
Upper Jay, NY Turkey I Turkey II Mt. Pamon, Greece
44’18’N/73”42’W 40°30’N/32”40’E 38’%0’N/28%0’E 41”05’N/23”25’E
1200 975 790
59.5 1 69.73 82.73 86.02
49.38 42.37(‘*) 36.58 35.97
84 83’12’ 60 70
77/v 70/v 66/v 75/v
Siberia Sweden North Italy Mayhill, NM
56”42’N/96”18’E 60”54’ N/ 16”30’E 46”18’N/l l”l8’E 33“OO’N/105°24’W
335 210 975 1950
52.84 59.45 73.43 60.80
28.35’*’ 31.39 44.20 43.28’15’
63’“’ 63 63. 90”s’
77/h 86/u 83/v 78/v
Recluse, WY Arnold, NE Reva, SD Toulnoustook R., Quebec
41°54’N/10S’36’W 41”24’N/100”00’W 45”36’N/103”12’W 49”42’N/68”24’
56.76 67.51 59.36 44.87
46.02 44.20 42.37 35.36(9)
100 97
W
1190 885 1050 75
77/v 73/u 72/v 82/u
Murray Bay, Quebec
47”36’N/70”
12’ W
90
51.08
33.53
96
83/u
Fort Coulonge., Quebec
45”48’N/76”42’
W
120
57.88
48.46
100
77/v
Mosinee, WI Mar1 Lake, MI Gladstone, MI Meeker, CO
44”48’N/89042’W 44”30’N/84”48’W 46”OO’N/86”3O’W 40°12’N/107”54’W
365 350 200 2500
56.95 54.54 53.95 51.94
48.16 46.63 45.11 35.05””
100 96 95 5811 1).
71/u 81/u 82/v 94/v
Durango, co Mayhill, NM Long Valley, AZ Eagle, CO Southwest CO. Garfield, UT. Mt. Nantai, Japan
37”30’N/ 107”48’ W 32”54‘N/ 105”24’ W 34”42’N/l ll”OO’W 39e3YN/106’55’W 37O4l’N/ 108’02’W 4C~~43’N/112~12’W 36’48’N/ 139’30’ E
2590 2135 2135 1980 2694 1320 1700
51.57 60.80 65.33 48.37 56.24 59.3 1 48.95
26.2 1 43.59 38.71 15.56’9’ 18.89 13.33 53.04t’3’
75 92
85 85 63’13’
92/u 86/u 89/v 84/u 81/u 77/u 73/v
Yatsuga, Japan Akaishi Mtns., Japan
35”54’N/138”18’E 35”24 N/ 138’06’E
1450 2000
52.23 45.67
65.53 63.40
81 79
86/u 73/v
Farm Island, SD BurweII, NE Centerville, KS
44”36’N/99036’W 42’3Y N/ lOO”O3 W 37”42’ N/94O08’ W
490 735 275
62.84 65.17 80.70
32.14”” 38.18 38.00
81 73
80(17J 59 93 84(” 9i
*(gk
;($
98’15’ 98 90
within
82/u 92/v 89/u 77/v 77/v
102/v 108/u 106/u
J.W. Zhnng.
B.M. Gregg/
Forest
Ecology
plant productivity. However, while photosynthesis has become easier to measure due to improved instrumentation, it is clear that the role of photosynthetic rate in plant growth has been overestimated (Khmer, 1991; Teskey et al., 1994). One of the important reasons for the lack of relationship between photosynthesis and growth is failure to measure net photosynthesis during the entire growing season (Teskey et al., 1994). Therefore, methods which provide an integrated measure of gas exchange, such as stable-carbon isotope discrimination, may explain variation in growth better than instantaneous measures. Plants discriminate against 13C when they fix carbon through photosynthesis (O’Leary, 1988) The isotopic signature in plant tissues is, therefore, influenced by both environmental variables and genetics (Farquhar et al., 1989). Measurement of carbon isotope discrimination in plant tissues ranks not only the plant’s water-use efficiency (WUE), defined as carbon gain to water loss (Farquhar and Richards, 19841, but also serves as a set point for gas exchange (Ehleringer, 1993). Moreover, discrimination gives an integrated measure for the period of time during which carbon is fixed. The technique may. therefore, be well suited to assess adaptedness of plants to environments. Carbon isotope discrimination varies among species in their natural habitats. Kijmer et al. (1988) and Khmer et al. (1991) demonstrated the variation when they sampled various species across the world, including annuals and perennials, evergreen and deciduous, trees and grasses, and so on. Furthermore, discrimination also differed between gymnosperms and angiosperms (Leavitt and Newberry, 1992; Garten and Taylor, 1992) and among species (Marshall and Zhang, 1994). Because these studies sampled trees in natural stands, the species differences in discrimination might be confounded with environmental effects. Provenance plantations provide a better opportunity to examine closely the genetic variation in carbon isotope discrimination
and Managemenr
83 (1996)
181-187
183
because they are well-designed and sufficiently replicated. In the present study, carbon isotope discrimination of foliage collected from the trees which grew from seeds originating from across the world was measured. The following questions are addressed: are there differences in carbon isotope discrimination among species or among provenances within species grown in a common garden? If so, how do the environmental variables in the seed source influence discrimination of the trees in the common garden? Finally, what are the relationships between carbon isotope discrimination and growth or survival?
2. Materials
and methods
The plantations are located at the University of Nebraska’s Homing State Farm, near Plattsmouth, Nebraska, USA (41”OO’N latitude, 95”54’W longitude, 335 m elevation). The trees grow on a silty loam soil derived from loess. The growing season averages 170 days, and mean annual precipitation is 760 mm of which about 75% falls during the growing season. All the species studied were conifers including Pinus strobus, P. strobifonnis, P. resinosa, P. nigra, P. sylvestris, P. ponderosa, P. banksiana, Pseudotsuga menziesii var. giauca, Picea pungens, Juniperus virginiana, and Lurix leptolepis. Of these species only Juniperus virginiana is native to east-
em Nebraska (Table 1). All the trees were propagated from seed collected in the native range of each species. Three or more provenances from each species and about six individual trees from each provenance were sampled. The number of trees were determined by coefficient of variation (CV) in carbon isotope discrimination of three conifer species in the previous study (Zhang, 1994) and statistical efficiency (Li et al., 1993). Current-year foliage was collected near the top of the crown using a bucket truck plus a 4 m pruning pole during October 1994.
Notes to Table 1: The plantations are located in Homing State Farm, NE, USA. The numbers in parenthesis are ages of plantations when these data were collected ET, evapotranspiration; AHG, annual height growth, WUE, water-use efficiency.
184
J.W. Zhng,
B.M. Gregg/Forest
Ecology
In the laboratory, two sub-samples were separated, one for measuring specific leaf area, another for carbon isotope discrimination. For the former subsamples, projected leaf areas were measured using Li-Cor leaf area meter (Li-Cor Inc., NE). The specific leaf area @LA) was calculated as projected leaf area (cm’) divided by leaf dry weight (8). For the second sub-samples, we dried the foliage at 70°C for 48 hours and ground it in a coffee mill to a fine powder. Relative abundance of 13C and ‘*C was determined with an isotope ratioing mass spectrometer at the Waikato Stable Isotope Unit, University of Waikato, New Zealand. The stable carbon ‘“C isotope ratio (S13C) was expressed as the 12 ratio C relative to PeeDee Belemnite (limestone) (Craig, 1957). The resulting 613C values were used to estimate isotope discrimination (A) as
and Management
83 (1996)
/81-I87
and King, 1990). Because height growth varied between stages of development (years), and ages of species (plantations) differed, 8-15 year height was used to calculate mean annual height growth (cm year- ’ >.
3. Results and discussion
Species differed in carbon isotope discrimination and specific leaf area (Fig. 1, P < 0.0001). Juniperus virginiana, which was only non-Pinaceae species in this study, had the lowest discrimination (I6.3%0) and SLA (22.0 cm* g- ‘>. Because this species grows in a wide range of climatic, edaphic, and topographic ranges (Van Haverbeke and Read, 1976), one might
A=- *a - *, 1 +6, where 6, is the isotopic composition of the plant material and 6, is that of the air (assumed to be - 8%0, Farquhar et al., 1989). Then “i is calculated following Farquhar’s model: A = 4.4 + 22.6”i
(2) ccl where ci is intercellular concentration of CO, and c, is atmospheric CO, concentration (355 ppm). Modelled WUE is estimated by: c, j+qJE=-
-
c;
(3)
1.6~ where u is the vapor pressure gradient between leaf and atmosphere. Climatic data were obtained from the National Oceanic and Atmospheric Administration (NOAA) (1994) for each provenance from the nearest weather station. Evapotranspiration for each provenance was calculated following Thornthwaite (1948). The growth and early survival data were collected from published literature on these provenances (Famsworth et al., 1972; Sprackling and Read, 1975; Van Haverbeke, 1983; Van Haverbeke, 1984; Van Haverbeke, 1986a; Van Haverbeke, 1986b; Van Haverbeke, 1987; Van Haverbeke, 1988; Van Have&eke
Species Fig. I. Species means and sta&ard error of specific leaf area aml carbon isotope discrimination in foliage of conifers grown in Homing State Farm, Nebraska, USA.
J. W. Zhang,
B.M. Gregg /Forest
Ecology
expect that natural selection shapes an adaptative strategy of Juniperus uirginiuna differently under various environments. In this study, all three provenances were from the Great Plains, where evaporation demand is usually high (Table 1). Therefore, selection for high WUE indicated by low discrimination may be high. Moreover, other species of Juniperus have been reported to have a lower discrimination than its sympatric species (cf. Marshall and Zhang, 1993). However, studying trees in southeast Wisconsin, Leavitt and Newbeny (1992) found that Juniperus viginiana and Pinus strobus had the same discrimination measured from cellulose (16.0%0); the result in this study, comparing the same species yielded discrimination of 16.3 and 18.%0 for Juniperus viginiana and Pinus strobus respectively. The difference between studies is not clear, but it may be that responses of both species vary to different environments. Another possibility is that because both studies analyzed different plant tissues (ccllulose vs. foliage), environmental factors may influence the products of biosynthesis (Kozlowski, 1992). Relatively low discrimination may also be related to the scale-like leaf in Juniperus. In a survey of native plants of the north-central Rocky Mountains, Marshall and Zhang (1994) found that Thuja plicata, also a scale-leaved evergreen, had the lowest discrimination. Although the mechanisms for scale leaf increasing WUEI is unknown, it may be that scale-like leaves with many xeromorphic characteristics (low specific leaf area, compacted and overlapped leaves, heavy cuticle, and small numbers of sunken stomata) increase resistance for water vapor to transpire from inside stomata to the atmosphere (Miller et al., 1995). Within the Pinaceae, discrimination of Pseudotsuga menziesii and Pinus strobiformis was among the lowest (17.9%0 and 18.2%0, respectively) and SLA was intermediate (42.0 cm’ g-’ and 43.5 cm2 g - ’ , respectively) of the species studied. Both species were grown from the seeds collected from the high elevations (> 2000 m> in the southern Rockies. The results differ from previous common-garden studies in that populations from high elevations had significantly high discrimination within the same species @hang et al., 1993; Zhang and Marshall, 1994; Zhang and Marshall, 1995). Clearly, an isotopic trend along an elevational gradient for populations within a species or for sympatric species is not
and Management
83 (1996)
181-l
87
185
appropriate to describe the trend for allopatric species because of genotype by environment interaction and the different magnitudes of phenotypic plasticity among species. Lurix leptolepis, a deciduous conifer, did not have the highest discrimination (19.1%0) as suggested by other studies (Gower and Richards, 1990; Zhang, 19941, but had the highest SLA (73.1 cm2 g-l) which is similar to other studies (cf. Gower and Richards, 1990). Because natural range of this species is only in an area about 200 km2 of the Japanese island Honshu, where evapotranspiration is low and annual precipitation is high ( = 1500 mm), one would expect the species to have a low WUE. However, when the species is grown in the Great Plains, where the climate is much drier and hotter than its native environment. Increasing WUE indicated by decreasing discrimination should, therefore, be expected, Within the pines, two members of the subgenus Hapoxylon, or soft pines (P. strobus and P. strobiformis) had lower A and higher SLA than five members of the Dipoxylon or hard pines (P. resinosu, nigra, sylvestris, ponderosa, and banksiana). Pines in the Hapoxylon are characterized by five-needle fascicles and one fibrovascular bundle (Little and Critchfield, 1969).This needle anatomy may be one of the features conserving water comparing to members of the Dipoxylon with two or three needle fascicle and two fibrovascular bundles. Within the hard pines, we found that the ranking of Pinus resinosa and P. banksiana in A were the same in our study as in the study of Leavitt and Newberry (1992). In the review of photosynthesis of pines across the world, Teskey et al. (1994) concluded that the responses of photosynthesis to most environmental factors were similar. In this study, the range of mean isotope discrimination among pines was from 18.18%0 to 19.83%0, which was much smaller than the range of in situ measurements. However, a 9% difference in discrimination equals 23% difference in modelled WUE (86.59/u and 70.39/u respectively) (Table 1). Because all trees were grown in the same environment, we would expect that net photosynthesis varied substantially among these pines during the period in which foliage was formed. Overall, variation in carbon isotope discrimination among provenances within species was significant
186
J.W. Zhang,
B.M. G-egg/Forest
Ecology
and Manqement
83 (1996)
181-187
Table 2 Correlation coefficients among annual height growth, carbon isotope discrimination, specific leaf area, and survival study site, and evapotranspiration and precipitation in seed source environments AHG A SLA Survival ET (cm year - ’ ) (a‘) (cm’ g- ‘) (o/o) (cm year ’ ) AHG (cm year- ’ J 0.60 * * I .oo 0.27 0.09 0.15 A (%c) I .oo 0.24 - 0.08 - 0.04 SLA (cm2 g- ‘J 1.00 -0.14 - 0.26 Survival (%) I a0 --0.16 ET (cm year- ’ ) 1.00 Precipitation (mm)
of trees grown on the Precipitation (mm? 0.67 _ ’ 0.24 0.66 - * -0.!9 -0.12 I.00
AHG, annual height growth; A. carbon isotope discrimination; SLA. specific leaf area; ET, evapotranspiration. * P < 0.01, which has been through Bonfetroni adjustment. l
(P = 0.035). Specific leaf area did not differ among provenances within species (P > 0.92). However, variation was substantial within some species such as Pinus nip-u (mean of A = 19.83, SE = 0.28), but not others such as Pinus resinosa (mean of A = 19.18, SE = 0.05). Similar results have been reported in Pseudotsuga menziesii and Larix occidentalis, but not in Pinus ponderosa (Zhang et al., 1993; Zhang and Marshall, 1994; Zhang and Marshall, 1995). It appears that genetic structures of carbon isotope discrimination are species specific. The correlations between carbon isotope discrimination and annual growth rate or survival were nonsignificant across the species (Table 2). No significant correlation was found between A and precipitation or evapotranspiration of the provenance although annual height growth, specific leaf area, and precipitation were intercorrelated. The result differed from the previous studies on single species or sympatric species in which. discrimination in the common-garden correlated with seed source climatic variables (Zhang, 1994). In the present study, distributions of species are far from one another and differences in environmental factors such as temperature and precipitation are much greater than that of A. Furthermore, many factors besides precipitation influence leaf gas exchange interactively. It is possible for a species to develop an unique adaptative mode in its own communities. Therefore, unlike studies of single species, no single trend can describe the responses of these species to various environments. In summary, carbon isotope discrimination differed significantly among species and among prove-
trances within species in the common garden. The correlations between the precipitation or evapotranspiration of the seed sources and discrimination were not significant. Because the species studied are adapted to widely disparate environments, we hypothesize that their genetic structures and acclimation processes are different. Selecting for better adapted genotypes based on carbon isotope discrimination must, therefore, be species specific.
Acknowledgements
We thank Ted Hovland and Darin Dauel for technical assistance, and two anonymous reviewers for their comments. The research was partially financed by USDA Cooperative State Research Service, NRI Competitive Grants #94-37100-0835 to BMC.
References Craig, H., 1957. Isotopic standards for carbon and oxygen and correlation factors for mass-spectromeuic analysis of carbon dioxide. Geochim. Cosmochim. Acta, 12: 133- 149. Ehleringer, J.R., 1993. Carbon and water relations in desert plants: an isotopic perspective. In: J.R. Ehleringer, A.E. Hall, and G.D. Farquhar @ditorsJ, Stable Isotopes and Plant CarbonWater Relations. Academic Press, New York, pp. 155-172. Farquhar, G.D., Ehleringer, J.R. and Hubick, K.T., 1389. Carbon isotope discrimination and photosynthesis. Annu. Rev. Piant Physiol. Plant Mol. Biol., 40: 503-537. Farquhar, G.D. and Richards, R.A., 1984. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust. J. Plant Physiol., 11: 539-552.
J.W.
Z/rang, B.M. Gregg/Forest
Ecology
Farnsworth, D.H., Gatherurn, GE., Jokela, J.J., Kriebel, H.B., Lester, D.T., Merritt, C., Pauley, S.S., Read, R.A., Sajdak, R.L. and Wright, J.W., 1972. Geographic variation in Japanese larch in north central United States plantations. Silvae Genet., 21: 139-147. Garten, C.T. and Taylor, G.E., 1992. Foliage 613C within a temperate deciduous forest-spatial, temporal, and species sources of variation. Oecologia, 90: l-7. Gower, S.T. and Richards, J.H., 1990. Larches: deciduous conifers in an evergreen world. Bioscience, 40: 818-827. Khmer, Ch., 1991. Some often overlooked plant characteristics as determinants of plant growth: a reconsideration. Funct. Ecol. 5: 162-173. Kijmer, Ch., Farquhar, G.D. and Roksaudic, Z., 1988. A global survey of carbon isotope discrimination in plants from high altitude. Gecologia, 74: 623-632. Kijmer, Ch., Farquhar, G.D. and Wong, S.C., 1991. Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Gecologia, 88: 30-40. Kozlowski, T.T. 1992. Carbohydrate sources and sinks in woody plants. Bot. Rev., 58: 107-222. Kramer, P.J., 1986. The role of physiology in forestry. Tree Physiol., 2: 1-6. Leavitt, S.W. and Newberry, T., 1992. Systematics of stablecarbon isotopic differences between gymnosperm and angiosperm trees. Plant Physiol. (Life Sci. Adv.), 11: 257-262. Li, X., Xu, J. and Zhu, Z., 1993. Optimum numbers of replication and plot size in forest tree field experimental design. J. Beijing For. Univ., 15: 103-111. Little, E.L. and Critchfield, W.B., 1%9. Subdivisions of the genus Pinus (Pines). USDA Forest Serv. Misc. Pub., 1144. Marshall, J.D. and Zhang, J.W., 1993. Altitudinal variation in carbon isotope discrimination by conifers. In: J.R. Ehleringer, A.E. Hall, and G.D. Farquhar (Editors), Stable Isotopes and Plant Carbon-Water Relations. Academic Press, New York, pp. 187- 199. Marshall, J.D. and Zhang, J.W.. 1994. Carbon isotope discrimination and water-use efficiency in native plants of the northcentral Rockies. Ecology, 75: 1887- 1895. Mi!ler, P.M., Eddleman, L.E. and Miller, J.M., 1995. Juniperus occidentalis juvenile foliage: advantages and disadvantages for a stress-tolerant, invasive conifer. Can. J. For. Res., 25: 470-479. O’Leary, M.H. 1988. Carbon isotopes in photosynthesis. BioScience, 38: 325-336.
and
Management 83 (1996) 181-187
187
Sprackling, J.A. and Read, R.A., 1975. Red pine provenance study in eastern Nebraska. USDA For. Serv. Res. Pap., RM16 7 pp. Teskey, R.O., Whitehead, D. and Linder, S., 1994. Photosynthesis and carbon gain by pines. Ecol. Bull., 43: 35-49. ‘Ihomthwaite, C.W., 1948. An approach toward a rational classification of climate. Geog. Rev., 38: 55-94. Van Haverbeke, D.F., 1983. Seventeen-year performance of Pinus jIexilis and P. srrobiformis progenies in eastern Nebraska. Silvae Genet., 32: 71-76. Van Haverbeke, D.F., 1984. Genetic variation in blue spruce: a test of populations in Nebraska. USDA For. Serv. Res. Pap., RM-253,6 pp. Van Haverbeke, D.F., 1986a. Twenty-year performances of Scotch, European black (Austrian), red, and jack pines in eastern Nebraska. USDA For. Serv. Res. Pap., RM-267, 14 pp. Van Haverbeke, D.F., 1986b. Genetic variation in ponderosa pine: a 15-year test of provenances in the Great Plains. USDA For. Serv. Res. Pap., RM-265, 16 pp. Van Have&eke, D.F., 1987. Genetic variation in Douglas-fir: a 20-year test of provenances in eastern Nebraska. USDA For. Serv. Res. Pap., RM-141, 8 pp. Van Haverbeke, D.F., 1988. Genetic variation in eastern white pine: a 15-year test of provenances in eastern Nebraska. USDA For. Serv. Res. Pap., RM-269, 7 pp. Van Haverbeke, D.F. and King, R.M., 1990. Genetic variation in Great Plains Juniperus. USDA For Serv. Res. Pap., RM-292, 8 PP. Van Have&eke, D.F. and Read, R.A., 1976. Genetics of eastern redcedar. USDA For. Serv. Res. Pap., WG-32, 17 pp. Zhang, J.W., 1994. Population variation in photosynthetic gas exchange, water-use efficiency, and carbon isotope. discrimination of three conifer species in western North America. Ph. D. dissertation, University of Idaho. Zhang, J.W. and Marshall, J.D., 1994. Population differences in water-use efficiency of well-watered and water-stressed westem larch seedlings. Can. J. For. Res., 24 92-99. Zhang, J.W. and Marshall, J.D.. 1995. Variation in carbon isotope discrimination and photosynthetic gas exchange among populations of Pseudorsuga menziesii and Pinus ponderosa in different environments. Funct. Ecol., 9: 402-412. Zhang, J.W., Marshall, J.D., and Jaquish, B.C., 1993. Genetic differentiation in carbon isotope discrimination and gas exchange in Pseudotsuga menziesii: a common garden experiment. Gecologia, 93: 80-87.
