Southern 

Research Station

Research Paper

SRS–48

United States

Department of

Agriculture

Forest Service

Fertilizer Responses of Volunteer 

Longleaf Pine Trees within a Loblolly 

Pine Plantation: Separating Direct 

Effects from Competition Effects

Peter H. Anderson and Kurt H. Johnsen
December 2009

Southern Research Station

200 W.T. Weaver Blvd.

Asheville, NC 28804

Authors: 

Peter H. Anderson, Research Biologist, and Kurt H. Johnsen, 

Research Physiologist, U.S. Forest Service, Southern Research 

Station, Durham, NC 27709.

Cover photo: Longleaf pine seedling Scotland County, 

NC, 2009. Photo by Peter H. Anderson.

DISCLAIMER

The use of trade or firm names in this publication is for reader information and does not imply 

endorsement by the U.S. Department of Agriculture of any product or service.
Abstract

Evidence is mixed on how well longleaf pine (Pinus palustris Mill.) 

responds to increased soil nitrogen via fertilization. We examined growth 

and physiological responses of volunteer longleaf pine trees within an 

intensive loblolly pine (P. taeda L.) fertilization experiment. Fertilizer 

was applied annually following thinning at age 8 years (late 1992) at rates 

tailored to maintain a high needle nitrogen concentration. We measured the 

annual growth of 20 volunteer longleaf pine trees per treatment. We took 

bimonthly gas exchange measures on 12 longleaf pine trees per treatment 

from June 1999 through June 2000, after which we estimated carbon 

isotope discrimination and foliar nitrogen concentration on foliage. The 

impact of fertilization in both growth and gas exchange was dependent on 

competition for light with neighboring loblolly pine trees. When fertilized 

longleaf pine trees were separated into categories with respect to being 

dominant or suppressed (relative to the loblolly pine trees) dominantfertilized trees had the lowest carbon isotope discrimination, increased 

photosynthesis, and decreased stomatal conductance, indicating greater 

water use efficiency in these trees. Compared to loblolly pine, longleaf 

pine growth is restricted less by poor soil nutrition. However, early rotation 

longleaf pine appears to have the potential to increase growth rate via 

fertilization to almost the same extent as loblolly pine. 

Keywords: Carbon isotopes, fertilization, growth, longleaf pine, 

photosynthesis, stomatal conductance.

Introduction

Longleaf pine (Pinus palustris Mill.) is an important conifer 

of the Southeastern United States Coastal Plain. Due to 

overexploitation, land use changes, and wildfire suppression, 

about 95 percent of the longleaf pine ecosystems have been 

eliminated since Europeans settled in the region (Landers 

and others 1995). Even so, enough of these pine systems 

remain to support an important industry for the Southeast in 

the removal of longleaf pine straw or litter for landscaping 

mulch. Often this removal is practiced on an annual basis. 

McLeod and others (1979) found significantly reduced 

growth of 16-year-old longleaf pine in South Carolina 

1 year after litter removal. While they found no decrease 

in macronutrients in needles formed after removal, it is 

reasonable to assume that litter removal reduces litter 

biomass and, thus, removes macronutrients from the soil 

Fertilizer Responses of Volunteer Longleaf Pine 

Trees within a Loblolly Pine Plantation: Separating 

Direct Effects from Competition Effects

Peter H. Anderson and Kurt H. Johnsen

around trees. It is unclear how continuous annual removals 

of litter organic matter will impact long-term site fertility 

and productivity, particularly in the deep sandy and infertile 

soils where longleaf pine often grow.

Commercial fertilization of southern pine stands has 

increased steadily over the decades with 1.2 million acres 

fertilized in 2004 (Fox and others 2006). Research has 

shown that fertilization increases productivity of loblolly 

pine (P. taeda L.) (Albaugh and others 1998, 2004), the 

most common southern pine species, but little research 

on fertilization responses of longleaf pine has been done. 

Because longleaf pine has adapted to sites with low nutrient 

availability, there has been a perception that longleaf pine is 

less responsive to fertilization than loblolly pine. However, 

longleaf pine straw biomass, foliar nitrogen (N), and 

phosphorous concentrations increased up to 50 percent 

2 years after fertilization, and fertilized trees in the sandhills 

of North Carolina had large percentage increases in both 

diameter and basal-area growth compared to controls (North 

Carolina State Forest Nutrition Cooperative 1998).

We examined growth and physiological responses of 

volunteer longleaf pine trees within an intensive loblolly 

pine fertilization experiment. We started fertilization 

treatments in 1992, when the trees were 8 years old, 

and continued annually for the 7 years of our study. The 

experimental loblolly pine planting was established on 

deep, well-drained sandy soil in 1985 following the harvest 

of a natural longleaf pine stand. We measured growth, 

photosynthetic gas exchange, and foliar carbon stable 

isotope discrimination. The objective of our study was 

to determine the impact of fertilization on the volunteer 

longleaf pines as well as the influence of competition of the 

crop loblolly pine trees on the responses. 

Materials and Methods

The study was conducted at the Southeast Tree Research 

and Education Site (SETRES), in the sandhills of Scotland 
2

County, NC (34°55′ N.; 79°30′ W.). SETRES sits on an 

infertile, excessively drained site that was once a naturally 

regenerated longleaf pine stand. The soil is mapped as a 

Wakulla series, which is highly permeable and well drained. 

Loblolly pine seedlings (1–0 containerized stock) were hand 

planted on 2 m × 3 m spacing in 1985 using a mix of 10 

open-pollinated families originating from the North Carolina 

Piedmont. The full SETRES study is a 2 × 2 factorial 

experiment with fertilization and irrigation treatments 

and four replicate blocks. Beginning in 1992, plots were 

thinned to 1,260 stems/ha and fertilizer was applied to 

achieve “optimum” foliar nutrition on fertilized plots. For 

the optimum nutrition treatment, N was applied annually in 

an attempt to achieve an N concentration in leaf dry matter 

of 1.3 percent with other macro- and micro-nutrients in 

balance; control foliar N concentration was approximately 

0.9 percent. Fertilization treatment goals have been achieved 

for the crop loblolly pine trees (Albaugh and others 1998). 

More details on the site, stand, and treatments can be found 

in Albaugh and others (1998, 2004).

We utilized only the nonirrigated control and fertilized plots 

where, on average, there were 41.3 (S.E. = 5.93) volunteer 

longleaf pine trees interspersed among the 1,136.7 

(S.E. = 83.5) loblolly pine stems/ha. Five longleaf pines 

per plot (20 per treatment) have been measured for height 

and diameter since 1992. A subset of 3 trees per plot (12 

per treatment) was measured for gas exchange bimonthly 

from June 24, 1999, through June 15, 2000. Measurements 

of net photosynthesis (Pn) and stomatal conductance (gwv) 

were conducted using a portable photosynthesis system 

(Model Licor 6400, Li-cor Inc., Lincoln, NE) on detached 

fascicles within 2 minutes from removal with a pole pruner. 

Fascicles were placed into the chamber while still attached 

to the removed shoot segment. On each date, measurements 

were made in the morning and in the afternoon on foliage 

collected from the upper and lower third of the crown of 

each tree. Measurements were conducted on sunny days, 

and light levels within the leaf chamber were set to ambient 

conditions.

Foliage samples were collected in October 2000 to 

estimate foliar N concentration and stable carbon 

isotope discrimination. First-flush foliage was collected 

from the upper, middle, and lower thirds of the 

crown from four trees per sample plot. Foliage from 

approximately 10 fascicles per sample were ground and 

analyzed for δ13C. Samples were analyzed for 13C:12C 

ratio using the Duke University, Phytotron SIRA 

Seriea II isotope ratio mass spectrometer (Micromass, 

Manchester, UK) operated in automatic trapping mode 

after combustion (SUMAS combustion) of samples 

in an elemental analyzer (NA1500 Series 1, Carla Erba 

Instrumentation, Milan, Italy). The reference carbon dioxide 

was standardized against standard Pee Dee belemnite. A 

system check of the combustion and mass spectrometer 

measurement was achieved with two interspersed (every 

10 samples) working standards of cellulose with a δ13C of 

–24.1±0.03 percent and –23.6±0.06 percent. The accuracy 

of δ13C with this analysis procedure is ±0.1 percent.

Due to the generally slow growth of the loblolly pine crop 

trees in the control plots, all volunteer longleaf pine trees in 

these plots had crowns in the dominant crown class. In the 

fertilized plots, due to the more rapid growth of the loblolly 

pine, seven of the longleaf pines trees were classified as 

dominant (comparable in height and diameter to neighbors) 

and five trees were classified as intermediate to suppressed 

(smaller than neighbors). Growth, gas exchange, and 

carbon isotope discrimination results were first analyzed via 

ANOVA using a randomized complete block design. Data 

was then analyzed using repeated measures ANOVA using 

a randomized split plot design (two treatments, four blocks), 

wherein this analysis fertilization regime is the whole 

plot and subplots were the three treatment classifications: 

control, dominant fertilized, and intermediate fertilized. 

Results

Seven years (1992–99) of annual fertilizer applications 

significantly increased height increment but not d.b.h. 

increment relative to control trees (table 1). Mean 1999 

height and d.b.h. of fertilized trees were not significantly 

different from controls. However, when fertilized trees were 

further split into intermediate and dominant crown classes, 

fertilization significantly increased height increment by

21 percent and d.b.h. increment by 18 percent in dominant 

trees, but suppressed-fertilized trees grew less than control 

trees after 7 years of annual fertilization.

Across all dates, Pn and gwv were significantly lower in 

fertilized compared to control trees in both the upper and 

lower crown (table 1). When crown classes were separated, 

these effects appeared stronger in suppressed trees but 

still generally occurred in dominant trees. Fertilized trees 

had more positive foliar δ13C values than control trees, 

indicating they had lower C isotope discrimination. When 

crown classes were separated, dominant-fertilized trees had 

higher δ13C values than intermediate-fertilized trees, which 

were higher than estimated from foliage of control trees. 

Mean δ13C and the Pn:gwv ratio from upper canopy needles, 
3

Table 1—Volunteer longleaf pine d.b.h. and height in December 1999; 1992–99 

d.b.h. and height increment; mean (all measurement dates) net photosynthesis (Pn ) 

(μmol/m2s, gs) of upper and lower canopy and needle conductance (gwv) (mol/m2/s); 

and foliar N concentration and δ13C from upper, middle, and lower canopy on 

foliage collected in October 1999 at Southeast Tree Research and Education Site, 

Scotland County, NC

* = significant difference between control and fertilized. 

Letters represent significant differences among control, fertilized (suppressed), and fertilized (dominant) trees.

Treatment

Fertilized 

(all)

Fertilized 

(suppressed)

Fertilized 

Trait Control (dominant)

N for growth measures 20 20 9 11

D.b.h. (cm) 13.72 13.94 12.1 15.04

(0.60) AB (0.65) (0.53) B (0.81) A

D.b.h. increment (cm) 8.24 9.22 8.03 9.93

(0.37) B (0.47) (0.52) B (0.61) A

Height (m) 10.05 10.16 9.45 10.69

(0.18) AB (0.30) (0.25) B (0.66) A

Height increment (cm) 6.17 6.98 6.5 7.27

(0.13) B * (0.24) (0.51) B (0.23) A

Foliar N (%) upper canopy 0.82 1.11 1.12 1.12

(0.03) B * (0.04) (0.07) A (0.05) A

Foliar N (%) mid canopy 0.79 1.03 1.06 1

(0.03) B * (0.05) (0.07) A (0.07) A

Foliar N (%) lower canopy 0.75 1.13 1.26 1.01

(0.03) C * (0.12) (0.20) A (0.07) B

N for physiology measures 12 12 5 7

Pn, upper canopy 3.67 2.99 2.85 3.1

(0.15) A* (0.17) (0.27) B (0.21) B

Pn. lower canopy 2.65 2.33 1.86 2.65

(0.11) A (0.15) (0.17) B (0.22) A

gwv, upper canopy 0.0415 0.0254 0.0254 0.0253

(0.0025) A* (0.0019) (0.0031) B (0.0023) B

gwv, lower canopy 0.0332 0.0207 0.0173 0.0232

(0.0022) A* (0.0017) (0.0021) B (0.0025) B

δ13C, upper canopy −27.65 −27.15 −27.56 −26.80

(0.20) A (0.33) (0.52) A (0.41) B

δ13C, middle canopy −28.28 −27.45 −27.78 −27.18

(0.28) A* (0.27) (0.43) AB (0.35) B

δ13C, lower canopy −28.69 −27.97 −28.28 −27.72

(0.19) A* (0.23) (0.37) AB (0.26) B
4

Figure 1— Relationship between the mean (across all measurement dates) ratio of 

net photosynthesis to needle conductance (Pn:gwv) with δ13C estimated for needles 

collected in October 1999 for upper canopy needles from control, suppressed 

fertilized, and dominant fertilized volunteer longleaf pine interspersed within a 

loblolly pine plantation.

as in intermediate trees. Values were lower than loblolly 

pine trees in both the control and fertilized treatments 

measured in a concurrent study (Gough and others 2004). 

Control longleaf pine foliar N was similar to values reported 

by Boyer and Miller (1994) but lower than what has been 

estimated as sufficient for commercial production of 

longleaf pine (Blevins and others 1996).

Across all dates, fertilization generally decreased rates of 

Pn and gwv in both dominant and intermediate longleaf pine. 

Although Murthy and others (1996) found that loblolly pine 

Pn increased the year after the fertilization treatment was 

initiated, Maier and others (2002) and Gough and others 

(2004) reported no impact effect or slightly lower rates of 

Pn due to fertilization after 4 and 6 years, respectively, of 

annual application, all at SETRES. It is likely that increased 

leaf area induced by fertilization was driving increased 

growth of longleaf pine, similar to what occurs in loblolly 

pine after an initial but brief increase in Pn rates (Gough and 

others 2004a, 2004b).

The lower gwv of fertilized trees is consistent with both 

theory (Ewers and others 2000, Gough and others 2004a) 

and empirical data (Ewers and others 1999, 2000), again 

tested on loblolly pine at SETRES. Fertilization on 

excessively drained sandy soil, without irrigation, reduces 

gwv by reducing the ratio of leaf mass to fine root mass 

which imposes water stress. This stress induces leaf and root 

by treatment/crown class, were positively correlated (fig. 1). 

Fertilization increased foliar N concentration, although not 

as much in dominant trees as in intermediate trees.

Discussion

Clearly, SETRES is an extremely nutrient deficient site; by 

the time this study was completed, nonfertilized 14-yearold loblolly pine winter foliar N concentrations were 

below 1.05 percent and peak projected leaf areas were 

below 2 m2/m-2 throughout the year. In the control plots, 

the volunteer longleaf pines on average grew 6.2 m over 

the 7-year study period, compared to 4 m for the control 

loblolly pine crop trees (Albaugh and others 2004). This 

supports the contention that longleaf pine is better adapted 

to nutritionally poor sites than loblolly pine (Harrington 

1990). Fertilization increased longleaf pine growth, but 

only when neighboring loblolly pine trees did not suppress 

the response. However, dominant longleaf pine trees grew 

an average of 7.3 m, compared to 8 m for the loblolly pine 

crop trees, over the 7-year study period (Albaugh and others 

2004). Thus, it appears that early rotation longleaf pine 

growth can be increased via fertilization to almost the same 

extent as loblolly pine. 

Fertilization increased foliar N concentration measured in 

October 2000 (table 1), but not as much in dominant trees 
5

tissue to develop with decreased specific conductivity and 

then more resistant to hydraulic failure from cell cavitation 

(Ewers and others 1999).

The larger reduction in gwv than Pn, caused by fertilization, 

increased the mean ratio of Pn:gwv, based on instantaneous 

gas exchange measurements. This result was consistent 

with foliar δ13C data. However, where light was not limited 

by competition with neighboring loblolly pine trees, the 

reduction in gwv due to fertilization did not result in a 

decrease in growth rate as would be expected if other factors 

were more or less equivalent (Farquhar and others 1982, 

1989).

Conclusions

Longleaf pine grew faster than loblolly pine on an 

excessively drained soil with low nutrition. In fertilized 

plots, the impact of fertilization of longleaf pine growth 

was dependent on competition with the crop loblolly pine 

trees. If longleaf pine was suppressed by neighboring 

loblolly pines, then overall growth after 7 years of annual 

fertilization was slower than control trees. However, 

nonsuppressed longleaf pine trees increased growth due to 

fertilization almost to the same extent as the loblolly pine 

trees. Annual fertilization increased longleaf pine foliar N 

but decreased Pn and, to larger extent gwv, increasing the 

Pn:gwv ratio. These analyses indicate that, at the time of 

the experiment, growth increases due to fertilization were 

not due to leaf level changes in physiology; they were 

likely due to increases in leaf area. These results may be 

partly attributed to competition effects with loblolly pine, 

which has responded positively (volume growth = 2.5 × 

controls) to fertilization. This suggests that longleaf pines 

grown in mixed plantations may have different fertilization 

requirements than when grown in pure stands. 

Acknowledgments

We thank John M. Seiler, Virginia Polytechnic Institute 

and State University, and S. Reza Pezeshki, University of 

Memphis, for their review of this article. We also thank 

Daniel McInnis, Chris Gough, and Luke McCall for help in 

data collection.

Literature Cited

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term growth responses of loblolly pine to optimal nutrient and water 

resource availability. Forest Ecology and Management. 192: 3–19.

Albaugh, T.J.: Allen, H.L.; Dougherty, P.M. [and others]. 1998. Leaf area 

and above- and below-ground growth responses of loblolly pine to 

nutrient and water additions. Forest Science. 44: 1–12.

Blevins, D.; Allen, H.L.; Colbert, S.; Gardner, W. 1996. Woodland owner 

notes - nutrient management for loblolly pine straw. WON 30. Raleigh, 

NC: North Carolina Cooperative Extension Service, North Carolina State 

University. 8 p.

Boyer, W.D.; Miller, J.H. 1994. Effect of burning and brush treatments on 

nutrient and soil physical properties in young longleaf pine stands. Forest 

Ecology and Management. 70: 311–318.

Ewers, B.E.; Oren, R.; Albaugh, T.J.; Dougherty, P.M. 1999. Carryover effects of water and nutrient supply on water use of Pinus taeda. 

Ecological Applications. 9: 513–525.

Ewers, B.E.; Oren, R.; Sperry, J.S. 2000. Influence of nutrient versus water 

supply on hydraulic architecture and water balance in Pinus taeda. Plant, 

Cell and Environment. 23: 1055–1066.

Farquhar, G.D.; Ehleringer, J.R.; Hubick, K.T. 1989. Carbon isotope 

discrimination and photosynthesis. Annual Review of Plant Physiology 

and Plant Molecular Biology. 40: 503–537.

Farquhar, G.D.; O’Leary, M.H.; Berry, J.A. 1982. On the relationship 

between carbon isotope discrimination and the intercellular carbon 

dioxide concentration in leaves. Australian Journal of Plant Physiology. 

9: 121–137.

Fox, T.R.; Allen, H.L.; Albaugh, T.J. [and others]. 2006. Forest fertilization 

in southern pine plantations. Better Crops. 90(3): 12–15.

Gough, C.M.; Seiler, J.R.; Johnsen, K.H.; Sampson, D.A. 2004a. Seasonal 

photosynthesis in fertilized and nonfertilized loblolly pine. Forest 

Science. 50: 1–9.

Gough, C.M.; Seiler, J.R.; Maier, C.A. 2004b. Short-term effects of 

fertilization on loblolly pine (Pinus taeda L.) physiology. Plant, Cell and 

Environment. 27: 876–886.

Guehl, J-M.; Fort, C.; Ferhi, A. 1995. Differential response of leaf 

conductance, carbon isotope discrimination and water use efficiency to 

nitrogen deficiency in maritime pine and pedunculate oak plants. New 

Phytologist. 131: 149–157.

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longleaf pine: model development and users guide. Gen.Tech. Rep. 

SO–80. New Orleans: U.S. Department of Agriculture Forest Service, 

Southern Forest Experiment Station. 28 p.

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of the Southeast: requiem or renaissance? Journal of Forestry. 

93(11): 39–44.

Maier, C.A.; Johnsen, K.H.; Butnor, J. [and others]. 2002. Branch growth 

and gas exchange in 13 year-old loblolly pine (Pinus taeda L.) trees in 

response to elevated CO2 and fertilization. Tree Physiology. 

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6

Murthy, R.; Dougherty, P.M.; Zarnoch, S.J.; Allen, H.L. 1996. Effect of 

carbon dioxide, fertilization and irrigation on photosynthetic capacity of 

loblolly pine trees. Tree Physiology. 16: 537–546.

North Carolina State Forest Nutrition Cooperative. 1998. Growth and 

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Anderson, Peter H; Johnsen, Kurt H. 2009. Fertilizer responses of longleaf pine trees 

 within a loblolly pine plantation: separating direct effects from competition effects.

 Res. Pap. SRS–48. Asheville, NC: U.S. Department of Agriculture Forest Service, Southern 

 Research Station. 6 p.

Evidence is mixed on how well longleaf pine (Pinus palustris Mill.) responds to increased soil 

nitrogen via fertilization. We examined growth and physiological responses of volunteer longleaf 

pine trees within an intensive loblolly pine (Pinus taeda L.) fertilization experiment. Fertilizer was 

applied annually following thinning at age 8 years (late 1992) at rates tailored to maintain a high 

needle nitrogen concentration. We measured the annual growth of 20 volunteer longleaf pine trees 

per treatment. We took bimonthly gas exchange measures on 12 longleaf pine trees per treatment 

from June 1999 through June 2000, after which we estimated carbon isotope discrimination 

and foliar nitrogen concentration on foliage. The impact of fertilization in both growth and gas 

exchange was dependent on competition for light with neighboring loblolly pine trees. When 

fertilized longleaf pine trees were separated into categories with respect to being dominant or 

suppressed (relative to the loblolly pine trees), dominant-fertilized trees had the lowest carbon 

isotope discrimination increased photosynthesis, and decreased stomatal conductance, indicating 

greater water use efficiency in these trees. Compared to loblolly pine, longleaf pine growth is 

restricted less by poor soil nutrition. However, early rotation longleaf pine appears to have the 

potential to increase growth rate via fertilization to almost the same extent as loblolly pine. 

Keywords: Carbon isotopes, fertilization, growth, longleaf pine, photosynthesis, stomatal 

conductance.
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