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1293 00793 75

This is to certify that the
dissertation entitled
Fine Root Production, Demography and Turnover
in Northern Hardwood Forests

presented by

Ronald L. Hendrick

has been accepted towards fulfillment
of the requirements for

 

 

Ph -D - degree in Fores‘trl

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Date q‘1g'q L

MSU is an Affirmative Action/Equal Opportunity Institution 0’ 12771

 

 

 

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PLACE IN RETURN BOX to remove this checkout from your record.
TO AVOID FINES return on or before dme due.

DATE DUE DATE DUE DATE DUE |

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

MSU Is An Affirmative Action/Equal Opportunity Institution
emunG-od

PINE ROOT PRODUCTION, DHNOGRAPHY AND TURNOVER
IN NORTHERN HARDWOOD PORSSTS

BY
Ronald L. Hendrick

A DISSERTATION

Submitted to Michigan state University
in partial fulfillment of the requirements
for the degree of

DOCTOR OP PHILOSOPHY

Department of forestry

1992

ABSTRACT
PINE ROOT PRODUCTION, DENOGRAPHY AND TURNOVBR
IN NORTHERN HARDWOOD PORESTS
BY
Ronald L. Hendrick

Data were collected from two sugar maple (Age; m
Marsh.) forests in 1989 and 1990. Direct observations of
fine root production, development and mortality were used in
conjunction with physical harvests of fine root biomass and
nitrogen content to measure root growth and death, and to
estimate the amount of carbon and nitrogen allocated to fine
root production and subsequently returned to the soil via

fine root turnover.

Analyses of cumulative survival distributions of
contemporaneous 1989 and 1990 cohorts revealed that roots at
the northern site consistently lived longer on average than
roots born during the same periods of time at the southern
site. The longer lifespan of roots in the northern forest
was due to significantly lower first-season mortality rates;
new roots were lost 64% faster at the southern forest (0.41
vs. 0.25 %'day'1, p <.01.). Overwinter and second-year
morality rates were not significantly different (p >0.5;
0.14 vs. 0.12 %°day'1) among the sites. Patterns of fine
root mortality at each site were the same for roots produced

at all times of the year, and our results suggest that

 

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temporal differences in biomass "turnover" may be due to
temporal variation in root production, not in root

mortality.

Greater than 50% of annual length production occurred before
mid—summer in both ecosystems, while the period of greatest
mortality was from late summer through winter. About 1/3 of
annual fine root. production and. mortality’ occurred
simultaneously, with little observable change in total root
length. Total fine root length observable in the

minirhizotrons peaked in mid-summer in both ecosystems.

Annual production values of approximately 8000 and 7300
kg'ha’yr'l were calculated at the Southern and Northern
sites, respectively, representing about 60% of total NPP in
both forests. Corresponding biomass mortality (i.e.
turnover) values were 6700 and 4800 kg'ha'yr‘l, and total
nitrogen returns to the soil from fine root mortality were
72 kg’ha'yr’1 at the Southern site and 54 kg'ha'yr'1 at the
Northern site. Fine roots dominated total biomass and N
litter inputs to the soil in both ecosystems, accounting for
over 55% of total biomass and nearly 50% of total N returns.
In both ecosystems, roots <0.5 mm comprised the bulk of fine
root biomass and N pools, and the contribution of these
roots to northern hardwood ecosystem carbon and nitrogen

budgets has probably been underestimated in the past.

S.

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91

me

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ACKNOWLEDGMENTS

Several individuals are responsible for helping me see this
work through to completion. I owe a special debt of thanks
to my major professor, Dr. Kurt Pregitzer, for his guidance
the past six years. I would like to thank him for his
advice, support and direction, as well as his willingness to
engage me in meaningful discussions, scientific and
otherwise, throughout my graduate program. Much of this
dissertation is a result of the free exchange of ideas and

criticisms that we have enjoyed the past several years.

I am indebted to the other members of my guidance committee,
Drs. Donald Dickmann, Robert Fogel, G. Philip Robertson and
Alvin Smucker, for their continuing advice and assistance.
Dr. Smucker was instrumental in exposing me to minirhizotron
technology and applications, and Dr. Fogel taught me a great
deal about roots and mycorrhizae while in the field and at
the Soil Biotron. Dr. Carl Ramm willingly provided
considerable statistical help and advice, for which I am
grateful. Drs. Donald Hall and Katherine Gross helped guide
me into the demography literature early in my studies, and I
thank them both. I would also like to express my gratitude
to my friend Dr. Phu Nguyen for his advice, encouragement

and willingness to assist me whenever I asked.

iv

 

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Melissa Moss deserves a special thanks for her tireless
efforts while digitizing minirhizotron images and sorting
root samples. .Andy Burton.‘was instrumental in helping
collect minirhizotron images and root samples, and was
responsible for much of the laboratory work getting done
properly and in a timely fashion. Bill Enslin wrote the
ROOTS program, and without ROOTS this work would not have
been possible. Several undergraduate laboratory assistants
helped in numerous ways, including Leslie Jagger, Lynn
Hanninen, Lori Grimm, Chiu Kwan Yu, Beth Palik and Wendy
Williams. I would also like to thank my colleagues Andy
Burton, Zhijun Liu and Brian Palik for their friendship,
advice and ability to carry on intellectually stimulating

discussions over a wide range topics.

Finally, I would like to thank my friends and family,
especially my parents, for their support and encouragement

throughout my studies.

TABLE OF CONTENTS

LIST OF
TABLESOOOOOOOOOOOOOO00......0......OOOOOOOOOOOOOOOOOOO.IViii

LIST OF FIGURES O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O I I x1
INTRODUCTION. 0 O O O O O O O O O O O O O O O O 0 O O O O O O I O O O O O O O O O O O O O ........ 1
CHAPTER

I. THE DEMOGRAPHY OF FINE ROOTS IN A NORTHERN
HARDWOOD FORESTOOOOOOO0.0.000000000000000000000lO

Abstract.....................................10
Introduction.................................12
Methods......................................17
Study Site and Minirhizotrons..............17
Image Analysis.............................21
Fine Root Life History, Longevity
and Dynamics..............................22
Results......................................24
Root Life History and Longevity............24
Root Production and Mortality (Turnover)...31
Discussion...................................37
Literature Cited.............................45

II. SPATIAL VARIATION IN TREE ROOT DISTRIBUTION
AND GROWTH ASSOCIATED WITH MINIRHIZOTRONS......49

Abstract.....................................48
Introduction.................................51
Methods......................................53
Results......................................57
Discussion...................................62
Literature Cited.............................67

III. PATTERNS OF FINE ROOT MORTALITY IN TWO SUGAR
MAPLE FORESTSOOOOOOOOCOOOCOOCOO0.00.0.000000000070

Abstract.....................................70
Introduction.................................71
Methods......................................72
Results and Discussion.......................75
Literature Cited.............................86

IV. THE DYNAMICS OF FINE ROOT LENGTH, BIOMASS AND
NITROGEN CONTENT IN TWO NORTHERN HARDWOOD
ECOSYSTEMSeeeeeeeeeeee eeeeeee eeeoeeeeoggooeeeeesg

Abstract........................... ....... ...89
Introduction.................................9l
Methods......................................94
Site Description...........................94
Fine Root Length Dynamics..... ..... ........97
Stand Biomass and Productivity.............99
Predicting Root Biomass Production
and Mortality............................103
Results.....................................104
Fine Root Length Dynamics.................104
Fine Root Biomass and Nitrogen Content....117
Production, Mortality and Standing Crop

Predictions..... ............. ............121
Discussion ....... .... ............. ..........128
Conclusions...... ........................ ...147

Literature Cited............................150

vii

Tab

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Table 1.1

Table 1.2

Table 1.3

Table 1.4

Table 2.1

LIST OF TABLES

Stand, soil and climatic characteristics of the
study site. Values are averages across plots,

with standard errors of the mean in parentheses
where shown ..... ............ ....... ...........18

Transition probabilities for roots in various
stages of development. P1, P2 and P are the
probabilities of a white root remaining white,
turning brown or dying during a given time
interval, respectively. P4 and P refer to the
probability of a brown root remaining alive and
brown or dying, respectively. Stage transitions
are depicted in Figure 1......................30

Periodic root length production and mortality
for total, white and brown root length. Values
are expressed as a percentage of the April 27,
1989 live root standing crop (plot mean) at both
<30 and >30-cm depths. Standard deviations are
given in parentheses..........................33

Initial root length standing crops, and the
production and mortality of total, white and
brown root length from April 27, 1989 to April
24, 1990 at <30 and >30 cm depths. Lengths are
plot averages in cm, with standard errors of the
mean in parentheses. (TOTAL length production
and mortality includes roots that first appeared
in a dead state, and thus the sum of WHITE and
BROWN production and mortality does not always
equal the TOTAL.).............................35

Analysis of initial root length, annual length
production, and annual production rate (annual
length production as a percentage of initial
root length), under three experimental
arrangements. Initial length and length
productgon are expressed in mm of root length
per cm' of minirhizotron viewing surface. Data
shown are means, standard deviations and
coefficients of variation.....................58

viii

Table

Table

Table

Table

Table

Table

Table

Table

Table

Table

Table

4.3

4.5

4.7

Stand, soil and climatic characteristics of the
study sites. Values are averages across plots,
with standard errors of the mean in parentheses
where shown...................................73

Birth intervals and size of root cohortsobserved
during the study........... ........ ...........74
Stand, soil and climatic characteristics of the
study sites. Values are averages across plots,
with standard errors of the mean in parentheses
where shown...................................95

Site means (and standard errors) of initial root
length density, annual length production and
annual mortality (April 1989 to April
1990)........................................1oe

Biomass and nitrogen content (kg'ha'l) of roots
<0.5, 0.5 to 2.0 and 2.0 to 10.0 mm in diameter,
as determined from soil cores. Plot means with
standard errors in parentheses...............118

Nitrogen concentration (%) of roots <0.5, 0.5 to
2.0 and 2.0 to 10.0 mm in diameter. Plot means
with standard errors in parentheses..........120

Comparison of measured and predicted total fine
(0.0-2.0 mm) root biomass and nitrogen content
standing crops, and predicted annual production
and mortality. Values are in kg‘ha'l, with
standard errors in parentheses...............122

Above- and belowground (less coarse roots >10
mm) April 1989 biomass, in kg'ha' . Plot means
with standard errors in parentheses..........124

Above- and belowground net primary production
(NPP), in kg'ha' 'yr- , for the period April
1989 through April 1990. Data are plot means,
with percentage of total NPP in
parentheses..................................126

Above and belowground litter biomass and N
returns to the soil from April 1989 to April
1990. Data are expressed in units of kg’ha' ,
and as a percentage of total litterfall. Plot
means with standard errors in parentheses....127

Comparison of fine root biomass and nitrogen
standing crops and annual production in some
North American deciduous forests. Biomass and N
standing crop and production values are in units
of kg'ha' and kg'ha' 'yr' , respectively....133

ix

Table 4.10 Annual fine root production per unit leaf weight
and leaf area in some temperate North American
deciduous forests. Leaf biomass data were
derived from published estimates of leaf litter
production................... ........ ... ..... 143

Figure

Figure

Figure

Figure

Figure

Figure

1.1

1.2

1.4

LIST OF FIGURES

Life cycle diagram for the fine roots of trees.

Pi’s are the probabilities of a root following a
particular path from one stage of development to
another during some time interval t...... ...... 16

Diagram of the minirhizotron, scribing and camera
system used to collect images. Components of the
camera and image recording system are labelled.
Item A is the minirhizotron itself, installed at
a 45° angle to the soil surface. Component B is
the camera, which records an image 1.8 cm wide by
1.2 cm in height. A blow-up of image frame 50 is
depicted in C, showing a scribed longitudinal
line along the left edge of the image and a small
numbered cross-hatch on this line. When filming,
the longitudinal line was aligned immediately
adjacent to the left edge of the image (as seen
in the monitor), and the cross hatch was centered
in the image using a reference mark on the
monitor........................................20

Initial distribution of root numbers among
diameter classes for the <30 and >30 cm depth
cohorts produced between April 27 and June 11,

1989.00.00.000000000000000.00.00.000...00......26

Initial root length distributions among diameter
classes for the <30 and >30 cm depth cohorts
produced between April 27 and June 11,

1989.00.00.00000000......OOOOOOOOOOOOOOOO0.0.0.27

Percent survival, with standard deviations, of
original root cohorts at <30 and >30 cm depths.
The proportion the remaining cohort comprised of
white and brown surviving roots is also shown.
The period of observation covers 346 days between
June 11, 1989 and May 23,

1990.00.00..................00.0.0000000000000028

Average soil moisture (15 and 75 cm depths) and
soil temperature (15 cm depth) during the 1989
and early 1900 growing seasons. Values are plot
averages.......................................32

xi

 

 

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Figure 2.1

Figure 2.2

Figure 3.1

Figure 3.2

Temporal changes in total, white and brown root
lengths (cm) at <30 and >30 cm depth, summed
across all plots. The period of observation
covers 363 days, from April 27 ,1989 to April 24,

1990.......OOOOOOOO......OOOCOOOOOOO......OO0.036

Relationship between initial root length
(27/4/89) in the upper 30-cm of soil and total
production during the following year, as viewed
with the minirhizotrons. Data shown are from 12
minirhizotrons, four within each of three
replicate plots................................60

Plot means, sampling (outer, wide bars) and
experimental (inner, narrow bars) error for
initial root length, annual length growth and
annual production as a percentage of initial
length. Units for Y-axis are in parentheses
below X-axis label for each estimate...........61

Root length survival curves for root cohorts
during 1989 and 1990. Survival times were
significantly greater at the northern site for
all but the July (no difference) and October
(southern site greater) 1989 cohorts. Cohorts
were comprised of all new roots present on the
minirhizotron surface that were produced between
successive sample dates in the upper 30 cm of the
soil. The data were pooled from the 12
minirhizotrons in each forest. Each root was
identified and numbered by the ROOTS image
analysis program we developed, and was remeasured
and classified as live or dead at each sampling
date. Significant differences in length survival
were tested usigg a Gehan-Mantel test for
censored data at an alpha of 0.05...........77

Regressions of length mortality data against the
number of days a cohort had been under
observation during it's first growing season,
with line forced through the origin. The slope
(mortality rate) of the southern site was
significantly greater than the northern site.
There were no site differences in over-winter and
second-year mortality rates (regressions not
shown). Data were pooled across all 1989 and
1990 cohorts. Differences among the two forests
were tested by comparing regression slopes at an
alpha of 0.05..................................79

xii

 

 

 

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Figure

Figure

Figure

Figure

Figure

Weekly averages for soil temperature at 15 cm
depth at both forests. Paired t-tests of site
differences in average weekly temperatures
(derived from the mean of three sensors at each
site) showed that temperatures from 26/4/89
through 17/10/89 and 30/4/90 through 16/10/90
were significantly greater at the southern site
(p <.001). Data were collected every 30 minutes
with an Omnidata monitoring system (Omnidata
International, Logan Utah, USA)................83

Total, white ang brown fine root length densities
(mm root per cm minirhizotron surface) at the
Southern and Northern sites from April 1989
through October 1990. Data are plot means with
standard error bars...........................106

Percentage distribution of total growing season
(April-October) fine root production and
mortality occurring between minirhizotron
sampling dates. April/May and May/June data in
1989 were calculated from April-early June and
early June-late June data by interpolation,
assuming that production and mortality were
evenly distributed during the 6 week interval
from late April to Early June at both sites...110

Percentage distribution of annual (April-April)
fine root production and mortality occurring
between minirhizotron sampling dates..........113

Cumulative (%) fine root production and mortality
at the Southern and Northern study sites. The
horizontal distance between the two curves at
each site is a relative index of turnover
time..........................................116

Cumulative diameter distribution of fine root
length and numbers at both study sites on the
July 1989 sampling date. Data represent values
summed across all plots: 587 roots and 3262 mm of
root at the Southern site, with corresponding
values of 662 and 4059 at the Northern site...136

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INTRODUCTION

Until the late 1970’s, little was known about the role of
fine roots in the carbon and nutrient economies of forest
ecosystems. The paper of Harris et al. (1977) from a
W W L. forest was probably the first
English-language report that specifically addressed fine
root production and mortality (i.e. turnover) in an
ecosystem context. Subsequent papers, many from coniferous
forests, soon followed (e.g. Cox et al. 1978, Fogel and Hunt
1979, Grier et al. 1981, Keyes and Grier 1981, McClaugherty
et al. 1982, Persson 1978, 1979), and fine root and
mycorrhizal production and turnover have now been studied in
several deciduous and coniferous forests worldwide (e.g.
Aber et al. 1985, Fogel and Hunt 1983, Gholz et al. 1986,
Gower et al. 1992, Hendrick and Pregitzer 1992, Joslin and
Henderson 1987, Nadelhoffer et al. 1985, Powell and Day

1991, Santantonio 1982, Vogt et al. 1982).

A consensus has emerged from these and other studies that
fine roots play a dominant role in the carbon and nutrient
budgets of most forests. Greater than one-half of annual
NPP is allocated belowground in many forests, and nutrient
fluxes to the soil from fine root mortality can be greater
than those from aboveground litterfall (Arthur and Fahey
1992, Cox et al. 1978, Fogel and Hunt 1979, Harris et al.

1977, Grier et al. 1981, Joslin and Henderson 1987, Keyes

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and Grier 1981, Vogt et al. 1986). However, many aspects of
fine root dynamics are still poorly understood. For
example, we know very little about fine root longevity (or
fine root life-history in general), even though measuring
longevity is key to quantifying carbon and nutrient fluxes
to and from fine roots. Given our poor understanding of
fine root longevity, it is not surprising that there is
considerable disagreement over the effects of soil resources
on rates of fine root turnover (i.e. Aber et al. 1985, Gower

et al. 1992, Reyes and Grier 1981, Nadelhoffer et a1. 1985).

Compounding these problems has been our inability to measure
the magnitude of concurrent fine root production and
mortality (Joslin and Henderson 1987, Kurz and Kimmins 1987,
Santantonio and Grace 1987). Because a physical sample of
roots can be destructively assayed only once, production and
mortality can be measured neither directly nor
independently, but must be inferred from changes in live
and/or dead fine root pool sizes. A high degree of spatial
variability in fine root biomass further exacerbates the
difficulties in measuring temporal variation in mass, and
hence root production and mortality. Small temporal changes
in root mass may be masked by random spatial variation
introduced by the heterogeneous nature of fine root
distribution, and the need to collect subsequent samples

from different locations in the soil.

 

 

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Close examination of these methodological difficulties
leaves little doubt that the destructive, discontinuous
methods typically used to study fine root dynamics are
largely responsible for our inability to make significant
new advances in our knowledge of fine roots (Fogel 1990,
Hendrick and Pregitzer 1992, Santantonio and Grace 1987,
Vogt et al. 1989). In contrast to traditional physical
sampling schemes, minirhizotrons offer the ability to study
fine roots ill-gig; in a non-destructive fashion. Because
the same roots can be monitored over extended periods of
time, spatial variability in fine root distribution becomes
fixed, and temporal dynamics can be measured directly and
more accurately (Atkinson 1985, Hendrick and Pregitzer
1992). The small size of minirhizotrons, and the
portability of the video systems used to collect
minirhizotron images, make them ideal tools for field
studies in remote, natural ecosystems. minirhizotrons have
already been used in several natural and managed plant
communities (Beyrouty et al. 1987, Cheng et al. 1990,
Eissenstat and Caldwell 1988, Hendrick and Pregitzer 1992,
Upchurch and Ritchie 1983), and their continued use in root

research seems likely.

Hinirhizotrons, however, suffer from limitations of their
own. The heterogeneous distribution of fine roots that has
long plagued destructive approaches can also lead to high

minirhizotron-to-minirhizotron variabil ity in root

 

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distribution. Coefficients of variation range up to as much
as several hundred percent (Merrill et al. 1987, Upchurch
and Ritchie 1983, Upchurch 1987) , and can make treatment
effects difficult to detect. Extracting data from
minirhizotron images has historically been a laborious, time
consuming process, although more automated methods of
analyzing minirhizotrons images are forthcoming (Smucker et
al. 1987). And, although there has been some success in
converting root length densities measured with
minirhizotrons to root biomass (Upchurch and Ritchie 1983,
Upchurch 1987), it is doubtful that minirhizotrons or other
direct observation techniques will replace destructive
sampling as a means to measure standing root biomass or

nutrient content.

The research reported in this dissertation is the result of
an attempt to: 1) more fully describe and quantify the
life-history and development of fine roots from their time
of birth until death, and 2) link direct observations of
root birth, growth and death with physical measurements of
root biomass and nutrient content to quantify carbon and
nutrient allocation to fine roots, and C and N returns to
the soil from fine root mortality. Secondary objectives of
this project were to increase the efficacy of minirhizotrons
as a means of measuring fine root dynamics, and to
facilitate the extraction and analysis of data from

minirhizotron images.

 

 

 

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The conceptual basis for this research lies in the premise
that a better knowledge of fine root demography (i.e. the
birth, development and death of individual fine roots and
root cohorts) is needed before we can make significant
advances in understanding the role of fine roots in
ecosystem processes. Demographic studies of leaves (Bazzaz
and Harper 1977, Hartnett and Bazzaz 1985, Maillette 1982a),
buds (Maillette 1982b), meristems (Porter 1983a,b) and
clonal ramets (Dickerman and Wetzel 1985) have proven useful
in research on aboveground plant parts, but this approach
has yet to be taken belowground, at least on a large scale.
The overall goal of this research, then, was to study fine
root demography at the ecosystem scale, and subsequently use
this information to quantify the role of fine roots in the C
and N cycles of Northern Hardwoods forests by linking modern
video technology with traditional ecosystem science

methodologies.

6

Literature cited

Aber, J.D. J.M. Melillo, R.J. Nadelhoffer, C.A. McClaugherty
and iJ. Pastor. 1985. Fine root turnover in forest
ecosystems in relation to quantity and form of nitrogen
availability: a comparison of two methods. Oecologia
66:317-321.

Arthur, M.A. and T.J. Fahey. 1992. Biomass and nutrients in
an Engelmann spruce - subalpine fir forest in north
central Colorado: pools, annual production and internal
cycling. Can. J. For. Res. 22:315-325.

Atkinson, D. 1985. Spatial and temporal aspects of root
distribution as indicated by the use of a root
observation laboratory. Pages 43-65 In: A.H. Fitter, D.
Atkinson, D.J. Read and M; USher, editors. Ecological
interactions in soil. Special Publication Number 4.
Blackwell Scientific, Oxford.

Bazzaz, F.A. and J.L. Harper. 1977. Demographic analysis of

the growth of Lgngm ugltgtiggimum. New Phytol. 78:193-
208.

Beyrouty, C.A., B.R. Fella, R.J. Norman, J.N. Marvel and
J.A. Pillow Jr. 1987. Characterization of rice roots
using a minirhizotron technique. In: (H.M. Taylor,
ed.) Minirhzotron Observation Tubes: Methods and
Applications for Measuring Rhizosphere Dynamics. pp 99-
108. American Society of Agronomy Special Publication
Number 50. American Society of Agronomy, Madison, WI.

Cheng, I., D.C. Coleman and. J.B. Box .Jr. 1990. Root
dynamics, production and distribution in agroecosystems
on the Georgia Piedmont using minirhizotrons. J. Appl.
Ecol. 27:592-604.

Cox, T.L., I.F. Harrie, 8.8. Asmua and N.T. Edwards. 1978.
The role of roots in biogeochemical cycles in an
eastern deciduous forest. Pedobiologia 18:264-271.

Dickerman, J.A. and R.G Wetzel. 1985. Clonal growth in Iyphg
Mia: population dynamics and demography of the
ramets. J. Ecol. 73:535-552.

Bieeenatat, D.M. and M.M. Caldwell. 1988. Seasonal timing of
root growth in favorable microsites. Ecology 69:870-
873.

7

Fogel, R. and G. Hunt. 1979. Fungal and arboreal biomass in
a western Oregon Douglas-fir ecosystem: distribution
patterns and turnover. Can. J. For. Res. 9:245-256.

Fogel, R. and G. Hunt. Contribution of mycorrhizae and soil
fungi to nutrient cycling in a Douglas-fir ecosystem.
Can. J. For. Res. 13:219-232.

Fogel, R. 1990. Root turnover’ and production in forest
trees. HortScience 25: 270-273

Gholz, R.L. L.C. Hendry and W.P. Cropper Jr. 1986. Organic
matter dynamics of fine roots in plantations of slash

pine (Rings 2111211111) in north Florida. Can J. For.
Res. 16:529-538.

Gower, 8.T., R.A. Vogt and C.C. Grier. 1992. Carbon dynamics
of Rocky Mountain Douglas-fir: influence of water and
nutrient availability. Ecol. Mono. 62:43-65.

Grier, C.C., R.A. Vogt, M.R. Reyes and R.L. Edmonds. 1981.
Biomass distribution and above- and belowground
production in young and mature M1139 3mm zone
ecosystems of the Western Cascades. Can. J. For. Res.
11:155-167.

Harris, I.F., R.G. Rinerson and N.T. Edwards. 1977.
Comparison of belowground biomass of natural deciduous
forests and loblolly pine plantations. Pedobiologia
17:369-381.

Hartnett, D.C. and F.A. Bazzaz . 1985 . The regulation of
leaf, ramet, and genet densities in experimental
populations of the rhizomatous perennial Sglidagg

ggnagengig. J. Ecol. 73:429-443.

Hendrick, R.L. and R.G. Pregitzer. 1992. The demography of
fine roots in a northern hardwood forest. Ecology
73:1094-1104.

Joslin, J.D. and G.8. Henderson. 1987 . Organic matter and
nutrients associated with fine root turnover in a white
oak stand. For. Sci. 33:330-346.

Reyes, H.R. and C.C. Grier. 1981. Above- and belowground net
production in 40 yr. old Douglas-fir stands on low and
high productivity sites. Can. J. For. Res. 11:599-605.

Rurs, I.A. and J.F. Rimmins. 1987. Analysis of error in
methods used to determine fine root production in
forest ecosystems: a simulation approach. Canadian
Journal of Forest Research 17:909-912.

8

Maillette, L. 1982a. Needle demography and growth pattern of
Corsican pine. Can. J. Bot. 60:105-116.

Maillette, L. 1982b. Structural dynamics of silver birch.
II. A matrix model of the bud population. J. Appl.
Ecol. 19:218-238.

McClaugherty, C.A., J.D. Aber and J.M. Melillo. 1982. The
role of fine roots in the organic matter and nitrogen
budgets of two forested ecosystems. Ecology 63:1481-
1490.

Merrill, 8.D., R.J. Doering and G.A. Reichman. 1987.
Application of a minirhizotron with flexible,
pressurized walls to a study of corn root growth. In
(H.M. Taylor, ed.) Minirhzotron Observation Tubes:
Methods and Applications for Measuring Rhizosphere
Dynamics. pp 131-143. American Society of Agronomy
Special Publication Number 50. American Society of
Agronomy, Madison, WI.

Nadelhoffer, R.J., J.D. Aber and J.M. Melillo. 1985. Fine
roots, net. primary’ production and nitrogen
availability: a new hypothesis. Ecology 66:1377-1390.

Persson, H.A. 1978. Root dynamics in a young Scots pine
stand in central Sweden. Oikos 30:508-519.

Persson, H.A. 1979. Fine root production, mortality and
decomposition in forest ecosystems. Vegetatio 41:101-
109.

Porter, J.R. 1983a. A modular approach to analysis of plant
growth. 1. Theory and principles. New Phytol. 94:183-
190. '

Porter, J.R. 1983b. A modular approach to analysis of plant
growth: II. Methods and results. New Phytol. 94:191-
200.

Powell, 8.W. and F.P. Day Jr. 1991. Root production in four
communities in the Great Dismal Swamp. Am. J. Bot.
78:288-297.

Santantonio, D. 1982. Production and turnover of fine roots
in a mature Douglas-fir stand in relation to site. Ph.D
Thesis. Oregon State Univ, Corvallis, OR.

Santantonio, D. and J.C. Grace. 1987. Estimating fine root
production and turnover from biomass and decomposition
data: a compartment flow' model. Can. J. For. Res.
17:900-908.

9

Bmucker, A.J.M., J.C. Ferguson, I.P. DeBruyn, R.R. Belford
and J.T. Ritchie. 1987. Image analysis of video-
recorded plant root systems. In: (H.M. Taylor, ed.)
Minirhzotron Observation Tubes: Methods and
Applications for Measuring Rhizosphere Dynamics. pp 99-
108. American Society of Agronomy Special Publication
Number 50. American Society of Agronomy, Madison, WI.

Upchurch, D.R. and J.T. Ritchie. 1983. Root observations
using a video recording system in minirhizotrons.
Agron. J. 75: 1009-1015 .

Upchurch, D.R. 1987. Conversion of minirhizotron-root
intersections to root length density. In: (H.M.
Taylor, ed.) Minirhzotron Observation Tubes: Methods
and Applications for Measuring Rhizosphere Dynamics. pp
51-66. American Society of Agronomy Special
Publication Number 50. American Society of Agronomy,
Madison, WI.

Vogt, M.A. C.C. Grier, C.H. Meier and R.L. Edmonds. 1982.
Mycorrhizal role in net primary production and nutrient
cycling in Abies amabilis ecosystems in western
Washington. Ecology 63:370-380.

Vogt. R.A, C.C. Grier and D.J Vogt. 1986. Production,

turnover and nutritional dynamics of above- and
belowground detritus of world forests. Adv. Ecol. Res.
15:303-307.

Vogt. R.A, D.J’ Vogt, 3.3. Moore and D.C. Sprugel. 1989.
Methodological considerations in measuring biomass,
production, respiration and nutrient resorption for
tree roots in natural ecosystems. pp 217-232. In:
(J.G. Torrey and L.J. Winship, eds.) Applications of
continuous and steady-state methods to root biology.
Kluwer. Dordrecht, Netherlands.

 

 

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Chapter I

THE DENOGRAPHY OF FINE ROOTS IN A NORTHERN HARDWOOD FOREST

Abstract

The production, development and mortality of fine roots in a
northern hardwood forest dominated by sugar maple (Age;
3921122931 Marsh.) was monitored for one year using
minirhizotrons. Roots were divided into two strata based
upon their depth in the soil, <30 cm and >30 cm. Cohort
analyses of roots produced in the spring of 1989 revealed
that while almost 50% of fine roots at both depths survived
after 346 days, the number of white roots in each cohort
declined very rapidly. Virtually all roots had turned brown
after 346 days. The probability of a surviving white root
turning brown was much greater than the probability that it
would die at all times of the year, and the bulk of root
mortality was accounted for by brown roots. Analysis of
root length production and mortality showed that total
annual length mortality at the <30 cm depth was 76% of the
initial standing crop and 110% at >30 cm depth. Fine root
production and mortality occurred simultaneously throughout
the year, and production was slightly greater than mortality
at both depths. Total root length peaked in the summer at
both depths, and overwinter production and mortality was

rather low.

10

11

Production of white and brown root length indicated that
roots near the soil surface were undergoing much more rapid
rates of browning than deep roots. Loss of root length
between sampling dates was largely due to roots that died

and rapidly decayed or otherwise disappeared.

12

Introduction

We have learned much about the contribution of roots to the
carbon and nutrient economy of forest ecosystems. For
example, greater than one-half of annual net primary
production is allocated belowground in some forests (Fogel
1985: Harris et al. 1977: Grier et al. 1981; Reyes and Grier
1981) . Fine (small diameter and/or non-woody) root
mortality can represent a substantial carbon and nutrient
input into the soil (Joslin and Henderson 1987: Cox et al.
1978) . The quantity of N added to the soil by root
mortality is from 18 to 58% greater than that added by
aboveground litterfall in some ecosystems (Vogt et al.
1986) . Mycorrhizae may also account for a substantial

portion of total belowground production (Fogel 1985).

The importance of understanding and quantifying the
processes influencing fine root dynamics (production,
longevity and mortality) has been recognized for some time
(Joslin and Henderson 1982, 1987: Kurz and Kimmins 1987:
McClaugherty et al. 1982: Nadelhoffer et al. 1985: Persson
1978) . Unfortunately, traditional sampling procedures do
not permit the simultaneous measurement of fine root
production, death and disappearance (Santantonio and Grace
1987: Kurz and Kimmins 1987) . Despite numerous

computational approaches that have been devised to

13

compensate for this difficulty (McClaugherty et al. 1982:
Joslin and Henderson 1982: Santantonio 1979), the
destructive nature of repeated soil coring renders the
direct measurement of these processes impossible.
Additional problems with destructive sampling include
differentiating between temporal differences in root
standing crops and artifacts of sampling variability (Singh
et al. 1984) , and separating live and dead roots (Fogel

1983, 1990).

Our incomplete understanding of fine root turnover is due in
part to our inability to quantify the demographic processes
underlying root dynamics. For example, we have a poor
understanding of fine root longevity, or how longevity is
influenced by the soil environment. Estimates of fine root
lifespans in forests range from less than one to greater
than eight years, depending on the size, species and
mycorrhizal status of the roots (Harris et al. 1977: Joslin
and Henderson 1987: Grier et al. 1981: Reyes and Grier
1981: Persson 1978, 1979, 1980: Santantonio 1979: Trappe and

Fogel 1977).

A more complete knowledge of fine root demography could
contribute to our understanding of several ecosystem
processes. The proportion of white roots that brown before
dying, versus those that die while still white, could affect

the quality of litter returned to the soil via root

14

turnover. We have previously documented substantial
differences in the N concentrations of white and brown fine
roots in sugar maple (Age: mm L.) (Goldfarb et al.
1990) . In that study we found that the N concentration in
brown roots averaged only about 60% that of white roots
throughout the growing season. If white (often
presumptuously called "unsuberized") roots are those most
important in nutrient and water uptake (but see Atkinson
1983, 1985) , then the rate and extent that roots age and
brown is also of considerable significance to canopy

processes like photosynthesis and transpiration.

Rhizotrons can be used to study root demography in 9.1131. and
to measure rates of root production and mortality directly.
This is more desirable than infering these rates from
estimates of biomass change. If the same roots and soil
space are monitored over time, temporal changes in root
dynamics are not confounded by random spatial variability at
each sampling date. Instead, spatial variability becomes
more or less fixed (Atkinson 1985) . Minirhizotrons are
useful for observational studies of roots in both natural
and managed ecosystems because of their small size and
accessibility. Several investigators have recently used
minirhizotrons to study root turnover in a variety of
agronomic and natural ecosystems (e.g. Beyrouty et al. 1987:
Cheng et al. 1990: Eissenstat and Caldwell 1988: Upchurch

and Ritchie 1983) . To our knowledge there are no

15

minirhizotron data from forests in the literature. The use
of minirhizotrons to study fine root production, development
and mortality (i.e. demography) should provide new insights

into the cycling of carbon and nutrients belowground.

The objectives of this research were to quantify several
demographic and life history traits of fine roots in a
deciduous forest, including their development and fate, as
well as the production and decline of white and brown root
length over time. For the purpose of this study, we
arbitrarily defined a fine root as any root less than 2.0 mm
in diameter. We were especially interested in the
demography of non-woody roots less than 1.0 mm in diameter.
Our belief is that a demographic approach to data collection
and analysis, coupled with minirhizotrons, can be used to
answer several simple but important questions. These
include: how long do fine roots live? To what extent are
root production and mortality continuous in time? What are
the typical stages of development in fine roots from
production to mortality? The conceptual framework on which

our questions were formulated is presented in Figure l.

16

 

 

 

. P3
WHITE —p- DEAD

 

 

 

 

 

 

 

 

 

BROWN » WOODY

 

 

 

 

 

 

Figure 1.1 Life cycle diagram for the fine roots of trees.
Pi's are the probabilities of a root following a particular
path from one stage of development to another during some
time interval t.

17

Methods

Study site and Minirhizotrons

Our study site is a hardwood forest located in the northern
lower peninsula of Michigan (Manistee County, 40° 42’ N, 85°
43' W), USA. The forest is a second growth stand dominated
by sugar maple (Age; sagggagum L., Table 1). The overstory
species, including their basal and leaf areas, are listed in
Table 1. Three 30 m by 30 m plots were established at the
site in 1987, selected so that a maximum degree of
homogeneity existed among them with respect to physiography,
soils and vegetation (Burton et al.1992). The herbaceous
community is depauperate, with an average cover value of
less than 3%. There are virtually no shrubs. The soil is a
Typic Haplorthod of the Blue Lake and Kalkaska series. A
number of stand and environmental variables were monitored
on each plot throughout the 1989 growing season. Percent
canopy foliation was determined periodically from prior to
bud break in the spring until after 100% leaf fall in the
autumn. Gravimetric soil moisture content was determined
monthly at 15 and 75 cm depths. Soil temperature at 15 cm
was recorded weekly with an Omnidata Easylogger (Omnidata

International, Logan UT).

Table 1.1
study site.

Stand,

18

soil and climatic characteristics of the
Values are averages across plots, with standard

errors of the mean in parentheses where shown.

 

 

General Stand Characteristics

Aboveground biomass (Mg'ha'l) 275
Overstory Age (yrs) 74 (11)
Canopy Height (m) 28 (1)
Budbreak (1989) May 9
100% Canopy Foliation (1989) May 23
50% Leaf Fall (1989) Oct 17
100% Leaf Fall (1989) Oct 30
Soil Variables (A+E Horizons)
pH (1:1 Water) 4.66(.27)
Bulk Density (g'Em'3) 1.27(.04)
Nitrogen (kg'ha' ) 1125(398)
Phosphorus (kg‘ha'l) 191(58)
Organic Matter (Mg'ha'l) 45.7(13.6)

Climatic Variables

30 Yr. Mean Annual Air Temperature (°C) 5.8
1989 Mean Annual Air temperature (°C) 4.7
Annual Precipitation (cm, 30 yr mean) 81
Growing degree Days (>5.6 C) 1944
Stand Composition
Bagal Area % Total Leaf Agea % Total
(m “ha" ) (m 'm )
Age; sacchagum 24.93 (0.50) 82.6 5.34 (0.34) 75.4
Age; rubrum 2.40 (0.74) 8.0 0.42 (0.13) 5.9
(Eruggs serotina 1.48 (1.07) 4.9 0.10 (0.05) 1.4
Quercus ggbra 1.35 (0.68) 4.5 0.95 (0.24) 13.4
.Eaggs grandifglia 0.03 (0.03) 0.1 0.14 (0.06) 2.0
{Total 30.19 (1.64) 100.0 7.08 (0.54) 100.0

 

19

In June 1988, 4 minirhizotrons (2 m long x 5.08 cm inside
diameter) were permanently installed in each plot at a 45°
angle to the soil surface, and to a depth of 165 cm along
their length (= 110 cm in vertical depth). The portion of
the minirhizotron extending above the soil surface was
painted and capped with a rubber stopper to prevent light
and rainfall from entering. Numbered image frames were
scribed onto the exterior surface of each minirhizotron
prior to installation so that we could return to the same
location within the minirhizotrons at all sampling dates. A
total of 130 frames were scribed, one every 1.2 cm (Figure
2). The image frames were oriented vertically during
installation. All minirhizotron images were collected on
VHS videotape with a Circon Microvideo 9011 Color
Agricultural Camera (Circon Co., Santa Barbara CA). The
camera is attached to a pole and jig assembly that is used
to control the depth and orientation of the camera lens in
the minirhizotron (Figure 2). Each minirhizotron was imaged
throughout the 1989 growing season, and imaging was resumed
in the spring of 1990 after snowmelt. The data presented in
this report were collected on 4/27, 6/11, 6/22, 7/18, 8/18,

9/16 and 10/14 in 1989, and on 4/24 and 5/23 in 1990.

20

 

 

 

 

 

 

 

 

 

 

 

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Figure 1.2 Diagram of the minirhizotron, scribing and
camera system used to collect images. Components of the
camera and image recording system are labelled. Item A is
the minirhizotron itself, installed at a 45° angle to the
soil surface. Component B is the camera, which records an
image 1.8 cm wide by 1.2 cm in height. A blow-up of image
frame 50 is depicted in C, showing a scribed longitudinal
line along the left edge of the image and a small numbered
cross-hatch on this line. When filming, the longitudinal
line was aligned immediately adjacent to the left edge of
the image (as seen in the monitor), and the cross hatch was
centered in the image using a reference mark on the monitor.

21

Image Analysis

An interactive PC-based software program (ROOTS) that we
have developed was used to analyze the minirhizotron video
images. A TARGA (Truevision Inc., Indianapolis IN) video
board was used in conjunction with ROOTS to digitize the
images from VHS tape, project them onto a computer monitor
and temporarily save them on-screen for processing. The
length and diameter of all roots present in each image was
traced using a mouse, and the measurements were
automatically calculated and written to a database file
(dBASE III+, Ashton-Tate, Torrance, CA) by ROOTS. The
tracings of each root were permanently saved by ROOTS on a
separate disk file. An identification code was assigned to
each root and written to the database. The code number was
derived from the order in which a root was traced within an
image (1, 2, 3, etc.): the frame (1-130), minirhizotron (l-
4) and plot (1-3) in which it was located: and the date on
which it was imaged (A-I) . The same code (except for the
collection date) was used for each root during the analysis
of subsequent images. We were able to identify the same
roots at subsequent dates by using ROOTS to recall and
overlay' the tracings and identification. numbers from. an
image at time t-l when analyzing time t images. Complete
records were kept for each root throughout its development,

even after it died and/or disappeared.

22

Each root was assigned a development stage code after it had
been traced. Roots were classified as "new" if they first
appeared in an image as white in color, and "white" at
subsequent dates if they remained white or cream in color.
Roots that turned, or first appeared as, tan to brown in
color were classified as "brown". Those that turned black
were classified as "dead". As roots decayed and
disappeared, or disappeared without first moving into a

"dead" state, they were classified as "missing".

When all the images from a given date had been analyzed, the
database records were compiled by minirhizotron and plot.
After images from all dates had been processed, the records
for the entire year were combined. The final database for
each. plot was a time series of lengths, diameters and

development stages for each root in all four minirhizotrons.

Fine Root Life History, Longevity and Dynamics

A cohort of roots produced between April 27 and June 11,
1989 was selected from each of two depths, (<30 cm, 194
roots and >30 cm, 140 roots), to study fine root development
and life history. All roots (summed across plots) produced
in this interval and still alive at the time of the June 11
observation were included in the cohorts. The mean root
diameter for each cohort was determined, as were the

frequency distributions (by diameter class) for root numbers

23

and root length. The development of the cohorts was
followed for a period of 346 days (June 11, 1989 to May 23,
1990) . The number of white roots moving into the brown,
dead or missing stages was determined for each time period,
as was the number of brown roots moving into the dead,
missing or woody stages. Brown roots were observed for
evidence of secondary vascular or cork cambial growth when

determining woody status.

The total number of roots alive at the end of each interval
was ‘used to icalculate percent. survival of' the original
cohort. Means and standard deviations were derived using a
formula (Cochran 1977) for estimating proportions from
cluster samples (cohorts) with unequal numbers of elements
(roots). Differences in final survival were tested using a
simple t-test (alpha = .01, Steel and Torrie 1980). The
probability of a root following any of the pathways depicted
in Figure 2 (remaining in stage i or moving to stage j) was
calculated by dividing the number of roots remaining in i or
moving to j during t to t+1 by the number in state i at time
t.

To calculate periodic and annual root production and
mortality, the white, brown and total (white + brown) root
lengths present on April 27, 1989 (time t = 0) were summed
for each plot by depth (<30 and >30 cm). Production and

loss of root length was followed for the next 363 days,

24

until April 24, 1990. The production of new white and brown
root length was calculated for the intervals t to t+1 by
summing the lengths of white and brown roots present at time
t+1 that were not present at time t, and adding the length
growth of existing roots. (All roots are white when first
produced, and brown root "production" during a given
interval actually reflects the browning of new white roots

during the same period).

Mortality was calculated by summing the length of roots that
moved into the dead or missing class during the same period,
plus the length of any roots that first appeared in a dead
state at time t+1. Percent production and mortality
estimates for the interval t to t+1 were calculated by
dividing the production and loss of white, brown and total
root length during the interval by the initial (April 27,
1989) standing crop. The mean and standard deviation of
each estimate was calculated using the method described

above for percent survival (Cochran 1977).
Results
Root Life History and Longevity
The average diameters of the <30 and >30 cm depth cohorts

were 0.42 mm (£0.18) and 0.49 mm (10.21), respectively. The

average diameter of the shallow cohort was less than that of

25

the deeper roots (t test alpha = .01), although the range of
diameters was similar for both cohorts: 0.18 - 1.55 mm for
the shallow cohort and 0.19 - 1.46 mm for the deep cohort.
The distribution of root length and numbers among diameter
classes was somewhat different between the cohorts (Figures
3 and 4). While 80% of root numbers and 76% of root length
in the shallow cohort was comprised of roots less than 0.50
mm diameter, the corresponding values for deeper roots were
only 64% and 56%. It is unlikely that many roots from
herbaceous species were included in the cohorts, due to the
very sparse ground layer in this stand (<3% total ground
coverage). Given the preponderance of sugar maple in the
overstory (83% BA and 75% of LAI), most of the roots we

observed probably belonged to this species.

The decline in numbers of live roots was greatest early in
the year at both depths (Figure 5). The mean 346 day
survival for roots at <30 cm depth was 47.4(16.8)%, greater
than that of 40.0(1-5.5)% for roots >30 cm deep (t-test,
alpha = .01). Most mortality was attributable to roots that
became missing before appearing dead. Of the 103 roots in
the shallow cohort that died, only one passed into a dead
stage before decaying or otherwise disappearing. At >30 cm,
eight of the 84 roots that died first occurred as dead,

rather than missing, roots.

26

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Figure 1.3 Initial distribution of root numbers among
diameter classes for the <30 and >30 cm depth cohorts
produced between April 27 and June 11, 1989.

 

 

 

 

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ROOT DIAMETER (mm)

Figure 1.4 Initial root length distributions among diameter
classes for the <30 and >30 cm. depth cohorts produced
between April 27 and June 11, 1989.

28

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Figure 1.5 Percent survival, with standard deviations, of
original root cohorts at <30 and >30 cm depths. The
proportion the remaining cohort comprised of white and brown
surviving roots is also shown. The period of observation
covers 346 days between June 11, 1989 and May 23, 1990.

29

The portion of the surviving cohort consisting of white and
brown roots changed considerably over time. Initially, both
cohorts were comprised primarily of white roots (128 of 194
roots <30 cm depth and 102 of 140 roots > 30 cm depth).
However, the portion of the cohorts comprised of white roots
dropped rather dramatically (Figure 5). By the end of
summer (125 days after the first observation), roughly 10%
of the roots were still white in both cohorts. After 346
days, no white roots remained in the deep cohort, while only
one of the roots from the shallow cohort remained white in

color.

The stage transition probabilities presented in Table 2 show
that white roots were most likely to remain in that state
between observation periods, rather than move to some other
stage. The chance of a white root dying (P3) was low
throughout the entire Observation period. The probability
of a white root turning brown (P2) was considerably greater
than the probability of it dying (P3) during all time
periods, regardless of depth. Browning probabilities were
greater for shallow roots during most of the growing season
(Table 2). Periods with high browning probabilities in the
shallow roots generally correspond to periods of low soil
moisture and high soil temperature at 15 cm (Figure 6).
Brown root mortality probabilities (P5) were greater for
deep roots during the summer, but were similar at both

depths from fall through spring. Brown root mortality was

Table 1.2
stages of development.

of a white root remaining white,
during a given time interval, respectively.

30

Transition probabilities for roots in various
P2 and P3 are the probabilities
turning brown or dying
P4 and P5 refer

to the probability of a brown root remaining alive and brown

or dying,

respectively.
graphically in Figure 1.

The stage transitions are depicted

 

 

JUN
JUL
AUG
SEP
OCT
APR

JUN

JUL
AUG
SEP
OCT
APR

TIME
PERIOD
11 - JUN
22 - JUL
18 - AUG
18 - SEP
16 - OCT
14 - APR
24 - MAY

TIME
PERIOD
11 - JUN
22 - JUL
18 - AUG
18 - SEP
16 - OCT
14 - APR
24 - MAY

22
18
16
16
14
24
23

22
18
16
16
14
24
23

0.76
0.58
0.68
0.66
0.68
0.12
0.50

0.84
0.74
0.77
0.63
0.52
0.19
0.00

0.17
0.39
0.32
0.32
0.28
0.82
0.50

>30 CM DEPTH

1’2

0.10
0.21
0.19
0.27
0.45
0.68
1.00

<30 CM DEPTH

0.07
0.03
0.00
0.03
0.04
0.06
0.00

0.06
0.05
0.05
0.10
0.03
0.13
0.00

0.95
0.95
0.92
0.95
0.81
0.74
0.93

0.97
0.88
0.88
0.90
0.81
0.66
0.91

0.05
0.05
0.08
0.06
0.19
0.26
0.07

0.03
0.12
0.12
0.10
0.19
0.34
0.09

 

 

31

greatest between Sept. 16 and Oct. 14 at both depths (Table
2), a period in which considerable leaf fall occurred (Table
1). The overwinter mortality probabilities were low for
white and brown roots at both depths. We did not observe
any roots in either cohort that developed obvious signs of
secondary growth during the 346 days the two cohorts were
followed.

Root Production and Mortality (Turnover)

Considerable root length was produced in the spring and
early summer of 1989 at both depths (Table 3), but very
little occurred from fall through. winter; Root length
production at the <30 cm depth was about evenly distributed
among white and brown roots from June 11 onward, except
during the period from July 18 to August 18, when there was
considerably more white root length produced. Soil moisture
increased rather substantially during this period (Figure
6). White length production was high for deep roots until
the end of summer, and then rapidly dropped off. There was
a considerable increase in the production of white root
length from July 18 to August 18 at >30 cm, just as there
was in the shallow roots. However, there was not a
corresponding increase in soil moisture at the 75 cm depth
(Figure 6). Other than during the first time period, brown
length production was spaced rather evenly throughout the

year at >30 cm. The annual production of white root length

32

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33

 

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uoou nacho one sauna .Heuou you xufiaeuuoa one co«uosooum summed poop Deccauom n.u eunea

34

was about 50% greater than brown length production at <30
cm, but was more than twice brown length production at the
greater depth (Table 4). As noted above (see Methods), all
roots are white when first produced, and high rates of brown
root "production" during a given interval actually reflect a
rapid browning of new roots during the same period. The
greater proportional production of white root length deeper
in the soil thus reflects a less rapid rate of browning at

greater depths.

Total shallow root mortality was more evenly distributed
throughout the year than was production, but increased
gradually from summer through fall (Table 3). There was
generally more total mortality at depths >30 cm, especially
towards the end of the growing season. The majority of
total root mortality at both depths was due to the loss of
brown root length (Tables 3 and 4). Overwinter length loss
was minimal at both depths (Table 3, Figure 7). Root length
peaked on August 18, 111 days after the first observation.
The decline from summer through fall was greater for deep
roots than shallow roots (Figure 7). Annual production was
greater than annual mortality at both depths (Table 4),

resulting in a net increase in total root length.

35

Table 1.4 Initial root length standing crops, and the
production and mortality of total, white and brown root
length from April 27, 1989 to April 24, 1990 at <30 and >30
cm depths. Lengths are plot averages in cm, with standard
errors of the mean in parentheses. (TOTAL length production
and mortality includes roots that first appeared in a dead
state, and thus the sum of WHITE and BROWN production and
mortality does not always equal the TOTAL.)

 

 

<30 CM DEPTH

TOTAL WHITE BROWN
Standing Crop 93.4 (6.0) 29.5 (9.9) 63.9 (5.8)
production 106.4 (10.9) 61.6 (11.8) 43.1 (7.1)
Mortality 76.5 (11.5) 12.1 (4.9) 62.6 (7.2)

>30 CM DEPTH

TOTAL WHITE BROWN
Standing Crop 57.1 (6.2) 31.8 (15.2) 25.3 (2.7)
Production 85.3 (10.3) 57.3 (13.6) 25.8 (3.2)

Mortality 69.8 (19.3) 20.5 (9.2) 47.1 (10.7)

 

36

[23 WHITE E BROWN H TOTAL

 

 

480.0

q

400.0": <30 cm DEPTH

320.03 D

.I

1
240.0-

160.09 , .
: //
80.05 .

q

O~Oy"‘~‘l’"‘/l""|""l""l""l""
0 50 100 150 200 250 300 .350

 

 

 

480.0

4100.0.- >30 cm DEPTH

320.01

..

240.0j

 

LIVE ROOT LENGTH (cm) — ALL PLOTS

160.0!

80.05

1
0,0 IIITIIIVIIIII liltilrllilillf

0 50 100 .160 ' ' 200 250 300 360
DAYS AFTER FIRST OBSERVED

Figure 1.7 Temporal changes in total, white and brown root
lengths (cm) at <30 and >30 cm depth, summed across all
plots. The period of observation covers 363 days, from
April 27 ,1989 to April 24, 1990.

 

 

 

37

Discussion

The distribution of root numbers and lengths suggests that
the shallow root system is, on average, comprised of thinner
(possibly longer) roots than the deep root system.
Silberbush and Barber (1983) suggested that a morphological
strategy favoring long, thin roots may be more effective
with respect to resource capture than one consisting of
shorter, thicker roots. In both cohorts most roots were
less than 0.5 mm in diameter, and most of the root length

consisted of roots of similar size.

White roots in the forest we studied are more likely to turn
brown than die at all times of the year (Figure 4). The
result is a rapid "loss" of white root length and numbers
from the cohorts, while total length and numbers change more
gradually. Our results also show that the fine roots of
deciduous trees can remain white considerably longer than
those of coniferous trees (Bartsch 1987). It is difficult
to place any functional significance on these results
because of our lack of understanding regarding physiological
differences between white and brown roots. Cortical
browning is temporally but not causally associated with the
process of suberization, and roots may be partially
suberized long before they turn brown (Richards and
Considine 1981: Johnson-Flanagan and Owens 1985). The

ability of "suberized" roots to absorb water to some extent

38

apparently exists (Kramer and Bullock 1966, Chung and Kramer
1975, Atkinson 1983, 1985), but. more sophisticated
experiments are needed for a greater understanding of
development and age associated changes in root function.
Only then can we link root form and function to aboveground
processes. The effects of root aging on carbon and nutrient
cycling belowground also cannot be ignored. We have
previously shown that sugar maple roots in this forest lose
about 40% of their N concentration upon browning (Goldfarb
et al. 1990). The fact that most fine root mortality is
attributable to the loss of brown roots suggests that
development-stage differences in root mortality probably
have a significant impact on the quality of litter returned

below ground.

The cohort survival data show that fine roots are capable of
relatively long-term survival. Few other estimates of root
longevity in deciduous forests are available in the
literature. However, if we assume that the lifespans of
fine roots are normally distributed, then one half of the
time required for the fine root pool to turnover once should
roughly equal the mean fine root lifespan. Under these
assumptions, the data of Nadlehoffer et al. (1985) yield a
mean lifespan of slightly more than 6 months for roots <3.0
mm in a Wisconsin sugar maple stand (turnover time = 0.94
yr). Visual inspection of the data of McClaugherty et al.

(1982) shows that the mass of roots <0.5. mm lost to

39

mortality each year in a mixed hardwood stand in
Massachusetts was around 100% of the standing crOp, equal to
an average fine root lifespan of about 6 months. Using data
from our study, the 76% annual length mortality of roots <30
cm in depth equates with a mean lifespan of 0.65 years, or 8
months. The corresponding value for roots >30 cm in depth
is 0.46 years, or 5.5 months. It appears from Figure 5 that
the mean lifespan of roots produced in the spring is closer
to 10 months (= time to 50% survival). Apparently there are
differences in the :mean longevity' of roots. produced at
different times of the year. To more accurately measure
fine root longevity it will be necessary to follow multiple
cohorts of roots produced at various times of the year until
all individuals have succumbed to mortality, an avenue we

are continuing to pursue.

In the shallow root system, most root production occurred
prior to August 18. Virtually no new root length was
produced from late fall through spring. White, brown and
total root mortality was spread rather evenly throughout the
year, other than a small peak between September 16 and
October 14 (Table 3). The data show that deep root
production was high through August, and declined
considerably thereafter. Conversely, almost half of total
root length was lost late in the year (Aug. 16 - Oct. 14),
when leaf senescence and the majority of leaf fall took

place (Table 1). The fall peak in shallow root mortality

40

also coincided with the period of greatest leaf senescence
(Tables 1 and 3) . There is apparently some degree of
temporal synchrony between leaf senescence and root
mortality, although we have no physiological data to suggest
a causal link between the two processes. While our data
permit little more than speculation at this point, the
possibility that fine root longevity is under strong

endogenous control deserves further study.

The seasonal trends in total live root length we observed
are in general agreement with patterns of fine root biomass
estimated from other North American deciduous forests.
Joslin and Henderson (1987) and McClaugherty et al. (1982)
measured late summer peaks for fine root biomass, as we did
for root length (Figure 7). We observed a substantial loss
of root length during late summer and autumn at both depths,
but minor overwinter losses of root length and numbers.
Joslin and Henderson (1987) and McClaugherty et al. (1982)
also observed a substantial autumnal decline in fine root
biomass. They and Nadelhoffer et al. (1985) all reported
minimal losses of root biomass during the winter months as

well.

Considerable production occurred throughout the growing
season at both depths (Table 2) . Likewise, substantial
amounts of root length were lost at both depths from spring

through late fall. These data confirm the statements of

41

others ( e.g. Fairley and Alexander 1985: Fogel 1985: Joslin
and Henderson 1987: Persson 1979) that estimates of fine
root production and turnover that do not accurately account
for concurrent production and mortality are potentially in
error. Substantial amounts of fine root production and
turnover do occur simultaneously, at least in the system we
studied, and temporal separation of these processes should
not be assumed in other ecosystems. Had we calculated root
length production based on the maximum difference in length
standing crops (sensu the min-max method of McClaugherty et
al. 1982) , our estimates for annual production would have
been 53 and 90% of the April 27 shallow and deep root length
standing crops, respectively. These numbers are
considerably less than the corresponding values of 107 and
136% we derived from direct observations of length growth

and production (Table 2).

A rather unexpected finding was the apparent rapid decay of
dead roots, as evidenced from the number and length of roots
that passed into the missing stage without first becoming
obviously dead. This phenomenon has been observed by others
working with rhizotrons of various types (R. Fogel, personal
communication) , and the mechanisms responsible need to be
identified. Movement of the minirhizotrons between
videotaping is unlikely because there should have been a
simultaneous disappearance of substantial numbers of roots

within a minirhizotron image, something we did not Observe.

42

The necessity that we use ROOTS to overlay the tracing of a
root from time t-l on its image at time t for our cohort
analyses revealed that temporal differences in camera

placement were generally much less than 0.5 mm.

Herbivory is an alternative explanation, but the available
literature would suggest that it is unlikely. Although many
groups of soil arthropods contain bacteria and fungal
feeders (Anderson and Ineson 1983: Richards 1987), little
importance has generally been ascribed to the invertebrate
fauna of forest soils as major consumers of live root tissue
(Ausmus et al. 1978: Fogel 1983, 1985: Magnussen and
Schlenius 1980). We see very little evidence of herbivory
in the form of partially eaten roots or fecal deposits on
the minirhizotrons. It must be acknowledged, however, that
knowledge of the composition and feeding biology of the soil
fauna is rather incomplete in most forest ecosystems,

including the one we studied.

Rapid decomposition after death seems to be the most likely
explanation for the disappearance of fine roots, although
one somewhat difficult to defend if published estimates of
root decomposition! are used as the benchmark, by which
minirhizotron observations are to be compared (McClaugherty
et al. 1984: Fahey et al. 1988: Joslin and Henderson 1987).
Present estimates of decomposition rates are considerably

slower than those we Observed in the minirhizotrons, and

43

resolving the two poses some difficulty. It is likely that
litterbag studies underestimate rates of decay to some
extent, as removing roots from the soil for washing, drying
and. ‘weighing severely' disturbs the rhizosphere and
rhizoplane communities. The effect of litterbag mesh size
must be considered (Fogel 1990: McClaugherty et al. 1984),
as small openings can restrict the entry of various
detritus-feeding invertebrates. Most of the roots we
observed were less than 0.50 mm in diameter, and the
difficulty of recovering these small roots from the soil may
result in litter samples that are biased towards larger,
more recalcitrant roots. It is also possible that the
readily available carbon supply (live and dead roots) on the
minirhizotron surface might stimulate rates of root decay by
attracting and supporting greater numbers of decomposers
than are found in non-rhizotron soil. In any event, the
rapid disappearance of roots from minirhizotrons deserves
further study. It is necessary that the discrepancy between
the rapid disappearance of roots from rhizotrons and the
rather’ slow’ decomposition. rates reported. by those using
buried bags be resolved. If the minirhizotrons give a more
accurate picture of the process of root decomposition than
buried bags, the ramifications for estimates of carbon and

nutrient cycling rates are considerable.

It is possible that the growth or development of the roots

we Observed could have been altered in some way due to the

44

presence of the minirhizotrons. The minirhizotron is a
rather inert surface, and may eliminate some biotic factor
(either adverse or beneficial) with which roots must contend
when growing through the soil. Ease of growth may also be
facilitated along the minirhizotron surface. However, the
general agreement of trends in our data with those derived
from destructive harvests suggests that any effect of the
minirhizotron is probably small. The fact that we were able
to observe and quantify phenomena that were previously
thought to occur (like the simultaneous production and
mortality of fine roots) suggests that minirhizotrons can be
of considerable use when addressing certain questions
concerned ‘with root dynamics. By linking direct
observations of fine root demography with simultaneous
measurements of root biomass, nutrient content and the soil
environment, a better understanding of the role of roots in

ecosystem processes should be possible.

45

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mechanistic mathematical model. Agronomy Journal 75:851-
854.

Steel, R.G.D. and J.R. Torrie. 1980. Principles and
Procedures of Statistics: A biometrical Approach. 2nd
ed. McGraw-Hill. 633 pp.

Trappe, J.M. and R. Fogel. 1977. Ecosystematic functions of
mycorrhizae. Pages 205-214 In: J.K. Marshall, editor.
The belowground ecosystem: a synthesis of plant-
associated processes. Range Science Department Science
Series Number 26, Colorado State University, Fort
Collins.

Upchurch, D.R. and J.T. Ritchie. 1983. Root observations
using a video recording system in minirhizotrons.
Agronomy Journal 75:1009-1015. -

Vogt, R.A, C.C. Grier and D.J. Vogt. 1986. Production,
turnover and nutritional dynamics of above-and
belowground detritus of world forests.. Advances in
Ecological Research 15:303-307.

Chapter II

SPATIAL VARIATION IN TREE ROOT DISTRIBUTION AND GROWTH

ASSOCIATED WITH MINIRHIZOTRONS

Abstract

Four minirhizotrons were installed in each of three
replicate plots in a deciduous forest dominated by Age:
eeeehezgm Marsh. The length growth of tree roots along the
surface of the minirhizotrons was measured for a period of
one year, and the resulting data were analyzed in nested,
averaged and pooled arrangements. The analyses of nested
data showed that spatial variation in root growth and
abundance among minirhizotrons within plots was greater than
variation among plots. Averaging data from minirhizotrons
within plots prior to analysis reduced variation about plot
means, but extensive intraplot variation invalidates this
approach on statistical grounds. Both nested and averaged
data failed to account for the contribution of individual
roots to the mean, and root production rates were
consequently overestimated. Pooling the data from the four
minirhizotrons reduced variation about the means, and
resulted in a more representative estimate of root
production rates. The analysis of composited data can be
used to incorporate small scale variation into a single

replicate sample in those circumstances where the activity

49

50

of the root systems of plant communities is the object of

study.

51

Introduction

Recent advances in microvideo technology have made
minirhizotrons popular research tools in both agronomic
(e.g. Cheng et al., 1990: Hansson and Andren, 1987: Keng,
1988: Upchurch and Ritchie 1983) and natural plant
communities (e.g Eissenstat and Caldwell, 1988: Hendrick and
Pregitzer 1992). During these and other research efforts,
several analytical and statistical problems with
minirhizotron data have been identified. High
minirhizotron-to-minirhizotron (i.e. spatial) variability in
root density and distribution has proven to be especially
problematic. Coefficients of variation range to as high as
several hundred percent (Merrill et al., 1987: Upchurch and
Ritchie, 1983: Upchurch 1987), often making treatment
effects (if any) difficult to Idetectn Quantifying and
controlling spatial variation is necessary to properly
execute minirhizotron experiments focused on root systems at
the level of the plant community or ecosystem, but
information on the extent of variation among minirhizotrons
at various levels within the hierarchy of an experimental

design is generally lacking.

Individual minirhizotrons are often the sampling units upon
which measurements of roots are made, and several
minirhizotrons are typically nested within replicate

experimental units, usually a field plot or greenhouse pot

52

(e.g. Beyrouty et al., 1987: Box and Johnson, 1987: Cheng et
al. 1990). Alternatively, minirhizotrons are sometimes
treated as experimental units, with measurements of root
numbers or length made along several different transects
(sampling units) within the minirhizotron (Eissenstat and
Caldwell, 1988: Gregory, 1979: Meyer and Barrs, 1985:
Sanders and Brown 1978) . Rarely, however, has the full
extent of among-sampling unit and among-experimental unit
variability in the data been reported. Instead, sampling
unit averages are the typical data upon which statistical

analyses are made.

As an alternative to analyzing sampling unit averages as
primary data, a few investigators have performed statistical
analyses on composited data from multiple minirhizotrons
(sampling units) within replicate experimental plots
(Hendrick and Pregitzer 1992) or from multiple transects
(sampling units) within replicate minirhizotrons (Hansson
and Andren 1987). Pooling minirhizotron data incorporates
spatial variation in root abundance and activity into a
single aggregate sample. Multiple samples within
experimental units are commonly pooled in studies of soil
and plant characteristics, but the assumptions and
implications of this practice in minirhizotron research have

not been discussed.

53

Our objectives in this paper are: 1) to more fully describe
the extent of spatial variation in tree root system
attributes: 2) to discuss the impact of analyzing the same
minirhizotron data under different experimental
arrangements: and 3) to suggest some ways to better control
spatial variability through analytical means. We have
extensive minirhizotron data on individual tree roots from
multiple ‘minirhizotrons (sample ‘units) within replicated
plots (experimental units), and hence the ability to analyze
minirhizotron data in a variety of experimental

arrangements.

Methods

Our study site is a second growth northern hardwoods stand
dominated by sugar maple (bee: W Marsh), and is
located in the northern lower peninsula of Michigan
(Manistee County, 40° 42' N, 85° 43' W), USA. The soil is a
Typic IHaplorthod. of‘ the Blue Lake and. Kalkaska series.
Three 30 m by 30 m analogous plots were established at the
site in 1987 (Burton et al. 1991). In June of 1988, 4
randomly located minirhizotrons (2 m long x 5.08 cm inside
diameter) were permanently installed in each plot at a 450
angle to the soil surface, and to a depth of 165 cm along
their length (110 cm in vertical depth). The portion of the
minirhizotron extending above the soil surface was painted

and capped with a rubber stopper to prevent rainfall and

54

light from entering. Numbered image frames were scribed
onto the exterior surface of each minirhizotron prior to
installation so that we could return to the same location
within the minirhizotrons at all sampling dates. A total of
130 frames were scribed, one every 1.2 cm. The image frames
were oriented vertically during installation. Minirhizotron
images were collected on VHS videotape with a Circon
Microvideo 9011 Color Agricultural Camera (Circon Co., Santa
Barbara CA). Each minirhizotron was imaged throughout the
1989 growing season, and imaging was resumed in the spring
of 1990 after snowmelt. The data presented in this report
were collected on 27/4, 11/6, 22/6, 18/7, 18/8, 16/9 and

14/10 in 1989, and on 24/4 and 23/5 in 1990.

An interactive PC-based software program (ROOTS) that we
have developed was used to analyze the minirhizotron video
images. A TARGA (Truevision Inc., Indianapolis IN) video
board was used in conjunction with ROOTS to digitize the
images from VHS tape, project them onto a computer monitor
and temporarily save them on-screen for processing. The
length of all roots present in each image was traced using a
mouse and written to a database file (dBASE III+, Ashton-
Tate, Torrance, CA) by ROOTS. Individual roots are defined
here as root segments present and visible within the
minirhizotron images. The tracings of each root were
permanently saved by ROOTS on a separate file. Each root

was classified as live or dead based upon its appearance.

55

Dead roots were distinguished from live roots by one or more
of the following characteristics: very dark brown or black
color, partial decay of the existing root and/or the
appearance and growth of fungal mycelia around the root.
Roots that completely' decayed and. disappeared. were

classified as "missing".

An identification code was assigned to each root and written
to the database. The code number was derived from the order
in which a root was traced within an image: the frame,
minirhizotron and plot in which it was located: and the date
on which it was imaged. The same code (except for the
collection date) was used for each root during the analysis
of subsequent images. We were able to identify the same
roots at successive dates by using ROOTS to recall and
overlay' the tracings and identification. numbers from. an
image at time t-1 when analyzing time t images. Complete
records were kept for each root throughout its development,
even after it died and/or disappeared. After the images
from all sampling dates had been processed for each
minirhizotron, the records for the entire year were
combined. The final database for each minirhizotron was a
time series of lengths and condition (live, dead or missing)
for each root. Data presented here are from the upper 30-cm

of the soil only.

56

To calculate root production, the total live root length
present on the first imaging date (27/4/89, t -= 0) was
summed for each minirhizotron. Root length production was
followed for the next 363 days (24/4/90). The production of
new root length was calculated for the intervals t to t+1 by
summing the lengths of new live or dead roots present at
time t+1 that were not present at time t, and then adding
the length growth of existing roots. Root "production" thus
includes both the growth of existing roots and the
production of new roots for a given time interval. Annual
root length production was calculated by summing the
production values for each observation period. The annual
production rate, expressed as a percentage of initial root
length, was calculated by dividing total annual length
production by the initial (27/4/89) root lengths.

The data were analyzed under three different experimental
arrangements: 1) a nested design with individual
minirhizotrons as subsamples within replicate plots (s=4,
r=3, n=12): 2) minirhizotrons as duplicates ‘within
replicated plots, with averages of the duplicates treated as
the primary data (n=3): and 3) data from each minirhizotron
pooled within replicate plots (n=3). To determine the
extent to which root length production rates were related to
the initial amount of root length present in each
minirhizotron, a correlation of total annual length

production with initial root length was made (n=12).

57

Results

A summary of the statistical analyses (Table 1) shows that
the same data, analyzed under different experimental
arrangements, can lead to different levels of variation
around estimates of the mean. The mean initial root length
densities (mm'cm'z) and root length production values
(mm'cm’z'yr) are the same regardless of the manner in which
the data were arranged prior to analysis. However, the
variation around the mean differs widely among the three
analyses. When data from individual minirhizotrons are
treated as samples within the replicated plots, coefficients
of variation (CV’s) for both initial root length density and
annual root length production are around 50%. (The standard
deviation in this arrangement was calculated from the
experimental, i.e among' plot, error ‘mean square of the
nested ANOVA: Steel and Torrie 1980.) Alternatively, when
the data from each minirhizotron are averaged by plot and
then analyzed, CV's for initial length and length production
are 11 and 21%, respectively: a considerable reduction in
variation” This improvement is not unexpected, as one
source of variation (among minirhizotrons within plots) has
been removed in this arrangement of the data. When
minirhizotron data are pooled by plot prior to analysis,
CV’s for initial length and annual production are the same

as those where the data is averaged over the tubes in each

58

Table 1. Analysis of initial root length, annual length
production, and annual production rate (annual length
production as a percentage of initial root length), under
three experimental arrangements. Initial length and l_e?gth
production are expressed in mm of root length per cm
minirhizotron viewing surface. Data shown are means,
standard deviations and coefficients of variation.

 

 

Minirhizotron Data as Subsamples within Plots (s=4, n=3)

NEED 52 £23
Initial length
(mm/cm'z) 3.57 2.02 56
Annual production
(mm/cm- ) 3.83 1.83 48
Annual prodpction
rate (%/yr' 131 76 58

Minirhizotron Data Averaged within Plots (n=3)

Meag SQ CV§
Initial length
(mm/cm'z) 3.57 0.40 11
Annual production
(mm/cm- ) 3.83 0.80 21
Annual prodpction 131 38 29
rate (%/yr

Minirhizotron Data Pooled within Plots (n=3)

Mean SQ CV§
Initial length
(mm/cm'z) 3.57 0.40 11
Annual production
(mm/cm- ) 3.83 0.80 21
Annual prodgction 106 11 10

rate (%/yr

 

59

plot. Again, within-plot variation among minirhizotrons has
been removed (combined into one sample) in this arrangement
of the data. The means of percentage production rates
differ among the three arrangements of the data (Table 1).
The means for the nested and averaged data were the same.
This was expected to be the case. The grand mean of n plot
means, each derived from m minirhizotrons, will be the same
as the overall mean of the nm minirhizotrons, provided that
the number of minirhizotrons in each experimental plot is

the same.

The production rate derived from the pooled data (106%) is
considerably lower than the rate derived via the other two
arrangements of the data (131%) . There was no apparent
relationship between the initial amount of root length
present in a minirhizotron and the amount of root length
produced along its surface (Figure 1). The Pearson product
moment coefficient between initial root length and annual
production was very low (0.008) and not significantly

different from zero (alpha = 0.05).

The results of the nested ANOVA of total root length, with
minirhizotrons as subsamples, are shown graphically (Figure
2). Variation in initial root length among minirhizotrons
within a plot (sampling error) was greater than the
variation) among' plots (experimental error). These data

suggest that the spatial distribution of tree roots in the

60

 

 

 

 

/~\ 500

2 e

3% e
Z

9 400‘“

F.

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8 300— r = .008
K ' a

Q_ .I

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E I '

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2i] 100- .

D

Z

Z

< O ' I f T

 

O 100 r 260 350 ‘ 4 D r 560 I 600
INITIAL ROOT LENGTH (MM)

tigure 2.1 Relationship between initial root length
(27/4/89) in the upper 30-cm of soil and total production
during the following year, as viewed with the
minirhizotrons. Data shown are from 12 minirhizotrons, four
within each of three replicate plots.

61

 

400
3504: “—

300€

 

 

250{ .

200?

 

150%

 

 

 

100‘
INITIAL LENGTH ANNUAL LENGTH ANNUAL LENGTH
(MM) PRODUGTK»I(MM) PRODUCHON
(7. INITIAL LENGTH)

rig. 2.2 Plot means, sampling (outer, wide bars) and
experimental (inner, narrow bars) error for initial root
length, annual length growth and and annual production as a
percentage of initial length. Units for Y-axis are in
parentheses below X-axis label for each estimate.

62

forest is highly variable over quite small areas; distances
between minirhizotrons within plots vary from one to several
meters, while plots are up to several 10’s of meters apart.
Length production and production rates show different
spatial patterns. Large scale (among plot) variation in
these variables is of approximately the same magnitude as

small scale (within plot) variation.

Discussion

There is no one right way to analyze all types of
minirhizotron data. Different experimental designs dictate
different statistical analyses, as do the hypotheses and
questions being addressed. However, general statistical
principles should guide the process of analyzing data from
an experiment in which the data are arranged in a nested or
hierarchical fashion. For example, if more than one
minirhizotron is sampled within each replicate experimental
unit, or if more than one transect is sampled in each
minirhizotron, the data should not be averaged prior to
analysis. Averaging data from transects within
minirhizotrons or minirhizotrons within plots is undesirable
unless variability among the sampling units is effectively
zero. However, our data (Figure 2) show that variability
among the minirhizotrons within our plots is considerable,
greater in fact than variation among plots. We suspect that

this may be true in other studies and experimental scenarios

63

as well. The loss of information on among-sampling unit
variability resulting from the analysis of averaged data
leads to a more conservative estimate of experimental error

and a greater risk of making a Type I error.

Instead of averaging, statistical analyses should be
performed on either nested or pooled data; perhaps both. A
nested ANOVA should always be performed first to ascertain
the extent of variation at both the experimental and
sampling unit levels. If sample unit variation is low
relative to variation among experimental units, only a
nested ANOVA should be performed; compositing or pooling the
data will have little effect on estimates of means and
variation. In these circumstances, the contribution of each
minirhizotron should be weighted by the number of roots or
amount of root length growing along its surface. If
sampling' error’ is large relative: to experimental error,
other options are available. It is possible to reduce
intraplot variation by computational means (without
increased replication) through an analysis of covariance
(ANCOVA) in a nested design if root abundance and activity
are related in a systematic fashion. However, abundance and
growth are rather uncoupled in the root system we studied

(Figure 1).

Increased replication or an adjustment in the number of

sampling units can also be employed. When sampling error is

64

greater than experimental error, standard analyses of design
efficiency are precluded and determining the proper number
of experimental units and the allocation of sampling units
among them can be difficult. It is apparent from our data
that little gain in precision would be made by increasing
the number of minirhizotrons within plots without a
concomitant increase in the number of plots. The formulas
presented by Sokal and Rolf (1981, pp 309-310) indicate that
to achieve a mean standard error of 20% for length growth at
our study site, a minimum of 5 replicate plots, each with 10
minirhizotrons, is required. This number is not excessively
high from a logistical standpoint, but might be financially
prohibitive if the cost of establishing replicate plots is
high (as was our experience) or if a large number of

experimental treatments are to be applied.

If deemed appropriate, data from multiple subsamples can be
pooled prior to analysis to reduce variation among
experimental units. Data should not be pooled as a matter
of standard practice. Since small scale variability is
incorporated into the estimate when compositing data, this
approach is not appropriate if quantifying the extent of
spatial variation in root distribution and activity is of
interest. However, when the root systems of plant
communities are the object of study, it is probably best to
have as much of the root system as possible in each

replicate sample.

One
tha'
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pr0<
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is 1
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and a.
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exhibi
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65

One of the primary advantages of analyzing pooled data is
that the effects of heterogeneous distributions of roots
among minirhizotrons are removed from estimates of
production and other means. We feel that a serious problem
with analyses of both averaged and non-weighted nested data
is the failure to consider the relative contribution of each
minirhizotron to the overall mean. Heterogeneous
distributions of roots among minirhizotrons can result from
many causes, including chance; various physical, biological
or chemical soil factors; differences in species abundance
and root morphology; inconsistencies in the minirhizotron-
soil interface: and possibly others. In analyses of pooled
or nested data, the result is that minirhizotrons with few
roots or little root length present contribute
proportionately more information to an estimate than do
minirhizotrons with a greater number of roots or root
length. This can be seen in our root production data (Table
1). The higher production rates associated with the nested
and averaged data resulted from the presence of at least one
minirhizotron per plot with a low initial root length
exhibiting a large relative amount of root production during
the year. The lower estimate of annual production derived
from the pooled data is likely to be a more representative
reflection of actual root system activity than the averaged
or nested estimates, since each root is given full

consideration in the pooled analysis.

objec
expel
acqu:
the

quesI

66

In summary, it is important that. we keep in. mind the
object(s) of interest when planning minirhizotron
experiments and subsequently analyzing the data. It is the
acquisition of better information on the average root, not
the average minirhizotron, that will help us answer our

questions about roots and root systems.

67

Literature Cited

Beyrouty, C.A., 8.1!. Wells, R.J. Norman, J.M. Marvel and
J.A. Pillow Jr. 1987. Characterization of rice roots
using a minirhizotron technique. In: Minirhizotron
Observation Tubes: Methods and Applications for
Measuring Rhizosphere Dynamics. Ed. M.M. Taylor. pp 99-
108. American Society of Agronomy Special Publication
Number 50. American Society of Agronomy, Madison, WI.

Box Jr., J.E. and J.M. Johnson. 1987. Minirhizotron rooting
comparisons of three wheat cultivars. In:
Minirhizotron Observation Tubes: Methods and
Applications for Measuring Rhizosphere Dynamics. Ed.
M.M. Taylor. pp 123-130. American Society of Agronomy
Special Publication Number 50. American Society of
Agronomy, Madison, WI.

Bragg, P.L., G. Govi and 3.9. Cannell. 1983. A comparison of
methods, including angled and vertical minirhizotrons,
for studying root growth and distribution in a spring
oat crop. Plant and Soil 73:435-440.

Burton, A.J. C.l. Ramm, x.s. Pregitzer and D.D. Reed. 1991.
Use of multivariate methods in forest research site
selection. Can. J. For. Res. 21:1573-1580.

Cheng, I., D.C. Coleman and J.E. Box Jr. 1990. Root
dynamics, production and distribution in agroecosystems
on the Georgia Piedmont using minirhizotrons. J. Appl.
Ecol. 27: 592-604.

Eissenstat, D.M. and M.M. Caldwell. 1988. Seasonal timing of

root growth in favorable microsites. Ecology 69:870-
873.
Fogel, R. 1990. Root turnover and production in forest

trees. HortScience 25:270-273

Gregory, PwJ. 1979. A periscope method for observing root
growth and distribution in field soil. J. Exp. Bot.
30:205-214.

Mansson, A.C. and o. Andren. 1987. Root dynamics in barley,
lucerne and meadow fescue investigated with a mini-
rhizotron technique. Plant and Soil 103:33-38.

Hendrick, R.L. and x.s. Pregitzer. 1992. The demography of
fine roots in a northern hardwood forest. Ecology
73:1094-1104.

68

Keng, R.C.I. 1988. Monitoring corn root development with a
mini-rhizotron in confined growth boxes. Argon. J.
80:287-291.

Levan, M.A., J.M. teas and J.M. Eummel. 1987. Light leak
effects on near-surface soybean rooting observed with
minirhizotrons. In: Minirhizotron Observation Tubes:
Methods and Applications for Measuring Rhizosphere
Dynamics. Ed. M.M. Taylor. pp 89-98. American Society
of Agronomy Special Publication Number 50. American
Society of Agronomy, Madison, WI.

Merrill, 8.D., E.J. Doering and G.A. Reichman. 1987.
Application of a minirhizotron with flexible,
pressurized walls to a study of corn root growth. In:
Minirhizotron. Observation Tubes: Methods and
Applications for Measuring Rhizosphere Dynamics. Ed.
M.M. Taylor. pp 131-143. American Society of Agronomy
Special Publication Number 50. American Society of
Agronomy, Madison, WI.

Meyer, LS. and 3.0. Barrs. 1985. Non-destructive
measurement of wheat roots in large undisturbed and
repacked clay soil cores. Plant and Soil 85:237-247.

Richards, J.R. 1984. Root growth response to defoliation in
two Agrgpyzgn bunch grasses: field observations with an
improved root periscope. Oecologia 64:21-25.

8anders,J.L. and 0.11. Brown. 1978. A new fiber optic
technique for measuring root growth of soybeans under
field conditions. Agron. J. 70:1073-1076.

Santantonio, D. and J.C. Grace. 1987. Estimating fine root
production and turnover from biomass and decomposition
data: a compartment flow model. Can. J. For. Res.
17:900-908.

Sokal, R.R. and F.J. Rolf. 1980. Biometry. 2nd. Ed. Freeman,
New York. 859 p.

Steel, R.G.D. and J.M. Torrie. 1980. Principles and
Procedures of Statistics: A biometrical Approach. 2nd
ed. McGraw-Hill, New York. 633 p.

Upchurch, D.R. and J.T. Ritchie. 1983. Root observations
using a video recording system in minirhizotrons.
Agron. J. 75:1009-1015.

0pch1

69

Upchurch, D.R. 1987. Conversion of minirhizotron-root
intersections to root length density. In:
Minirhizotron Observation Tubes : Methods and
Applications for Measuring Rhizosphere Dynamics. Ed.
M.M. Taylor. pp 51-66. American Society of Agronomy
Special Publication Number 50. American Society of
Agronomy, Madison, WI.

PAT

The

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temp
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insi
fore

Of 9

Chapter III

PATTERNS OF FINE ROOT MORTALITY IN TWO SUGAR MAPLE FORESTS

Abstract

The survival of contemporaneous root cohorts produced during
succesive intervals of time was followed in two sugar maple
(Age; saccharum Marsh.) forests for a period of two years.
Analyses of the survival distributions of the cohorts showed
that roots in the northern forest consistently lived longer
than those in the southern forest. Differences were due
principally to much greater rates of mortality early in the
life of roots at the southern site; overwinter and second-
year mortality rates were the same at both forests. An
examination of site factors suggests that warmer soil
temperatures seem to be associated with the more rapid rates
of root death at the southern site. The results provide new
insights into fine root dynamics in ‘temperate deciduous
forests, and have important implications for future studies

of ecosystem productivity and carbon and nutrient cycling.

7O

71

Introduction

A large proportion of the carbon assimilated by plants is
allocated to fine root production (Gower et al. 1992, Grier
et al. 1981, Keyes and Grier 1981, Harris et al. 1977, Fogel
1985), and the flux of carbon and nutrients to the soil from
fine root mortality is as much or greater than that returned
via leaf litter in many forests (Cox et al. 1978, Joslin and
Henderson 1987, Raich and Nadelhoffer 1989, Vogt et al.
1986). However, our knowledge of the demographic processes
underlying the dynamic nature of fine roots is incomplete,
in large part because of limitations inherent in traditional
methods of studying root systems. Given the importance of
roots in ecosystem carbon and nutrient budgets, a better
understanding of fine root mortality would improve our
attempts to quantify broad-scale carbon budgets and model
plant ecosystem processes (Raich and Nadelhoffer 1989, Vogt
et al. 1986, Ewel and Gholz 1991, Landsberg et al. 1991).
Here we present the results of an observational study
utilizing recent advances in microvideo technology (Hendrick
and Pregitzer 1992a, Upchurch and Ritchie 1983) in which we
followed the mortality of fine root cohorts in two similar
sugar maple (Age; gagghgzum Marsh.) forests during 1989 and

1990.

In

(nix
forI
The]
mat1
nit:
1992
cont
lea:
1985
1991

of 1

72

Methods

In June 1988 we installed 12 clear, 5-cm diameter tubes
(minirhizotrons) in each of two closely matched sugar maple
forests (Table 1) located 80 km apart from north to south.
There are no appreciable site differences in soil organic
matter content, cation exchange capacity/saturation, total
nitrogen (N), exchangeable Ca Mg, Al or K (MacDonald et al.
1991), N mineralization or growing season soil moisture
content, and there were no significant differences in canopy
leaf area, litterfall production or litterfall N in either
1989 or 1990 (Burton et al. 1991, Pregitzer and Burton
1991). We used a microvideo camera to record monthly images
of fine root cohorts growing in the top 30 cm of the soil
along a 1.8-cm-wide transect on the minirhizotron surface
during the 1989 and 1990 growing seasons. Cohorts were
comprised of all living fine roots 1.5 mm in diameter or
less, pooled across the 12 minirhizotrons (Hendrick and
Pregitzer 1992b), that were produced during the intervals
between sampling dates (Table 2). We used a microcomputer
software program (ROOTS, Atkinson 1992, Hendrick and
Pregitzer 1992a) to identify and. measure the length of
individual roots within contemporaneous cohorts at each
site, and subsequently follow their fate by repeatedly

measuring the same roots at each sampling date.

TablI
stud:
stanI

 

 

Lati
Long
Abov

Over
Basa
Suga
Cano
Leaf

Mean
Mean
Grow
Mean

73

Table 3.1
study sites.

across

Stand, soil and climatic characteristics of the

Values are averages plots, with

standard errors of the mean in parentheses where shown.

 

 

Latitude
Longitude
Aboveground biomass (Mg'ha'l)

Overstory Age (yrs)
Basal Area (m 'ha'l)
Sugar Maple Basal Area (%)
Canopy Height (m)
Leaf Area Index (mz/mz)
1989
1990
Mean Annual Air Temperature (°C)
Mean Annual Precipitation 6mm)
Growing degree Days (>5.6 C)
Mean Spring - Fall Soil
Temperature (°C at 15 cm)
26/4/89 - 17/10/89
(3.5)
30/4/90 - 16/10/90

Va les A+ o ' 0

pH (1:1 Water)

Bulk Density (g'im'3)

Nitrogen (kg'ha' )

N Mineralization (Tg°kg'1'yr'l)
Phosphorus (kg'ha- )

Organic Matter (Mg'ha'l)

Southern
EQ£§§§

43°40'
86°09’
234

78 (5)
30 (2.0)
75 (13)
24 (1)

9 (0.3)
.7 (0.4)
5
0

14.2 (4.3)

14.6 (3.3)

4.66(.46)
1.27(.07)
1408(100)
134.4
156(18)
41.7(3.3)

Northern

Forest

44°23'
85°50’
275

74 (11)
30 (2.8)
83 (5)
28 (1)

12.9 (3.2)

4.66(.27)
1.27(.04)
1125(398)
100.8
191(58)
45.7(13.6)

 

 

1989

25/4

7/6
21/6
18/7
16/8
16/9

1990

14/1
25/
24/
18/
21/
18/
18/

74

Table 3.2 Birth intervals and size (numbers and length in
mm) of root cohorts observed during the study.

 

 

Southern Forest Northern Forest

Birth Birth

Interga; fi’s Length Integya; fi's Length

1989: 1989:

25/4 - 7/6 152 793 29/4 - 11/6 196 1074
7/6 21/6 87 342 11/6 22/6 78 398

21/6 18/7 105 357 22/6 18/7 85 390

18/7 16/8 70 274 18/7 16/8 108 493

16/8 16/9 97 376 16/8 16/9 64 262

16/9 - 14/10 56 223 16/9 - 14/10 26 103

1990: 1990:

14/10 - 25/4 55 211 14/10 - 24/4 31 185
25/4 - 24/5 97 363 24/4 - 23/5 30 183
24/5 - 18/6 88 318 23/5 - 19/6 245 1135
18/6 - 21/7 102 421 19/6 - 22/7 58 225
21/7 - 18/8 95 307 22/7 - 19/8 61 285
18/8 - 18/9 57 170 19/8 - 19/9 56 305
18/9 - 16/10 56 217 19/9 - 26/10 61 298

 

Our 0b
mortali
hypothe
similar
charact
root lj
Mantel

distrit
reveals
longer

time a
excepti
and Se;
l°nger

Signifj
Regres

days 8:
were 1
%°day‘

rates

 

0.12 %
I

The 9.
Simil.

(P180

75

Results and Discussion

Our objectives were to quantify patterns of fine root
mortality in these two closely matched ecosystems. We
hypothesized that fine root length would be lost at a
similar rate in both forests because of the similar site
characteristics. However, we found large differences in
root lifespans between the two forests (Figure 1).. Gehan-
Mantel (Pyke and Thompson 1986) tests of cumulative survival
distributions of contemporaneous 1989 and 1990 cohorts
revealed that roots at the northern site consistently lived
longer on average than roots born during the same periods of
time at the southern site (alpha = 0.05). The only
exceptions were two 1989 cohorts; July (no site differences)
and September (greater longevity at the southern site). The
longer lifespan of roots in the northern forest was due to
significantly lower first-season mortality rates (Figure 2).
Regressions of root length survival against the number of
days since a cohort was first observed showed that new roots
were lost 64% faster at the southern forest (0.41 vs. 0.25
%'day'1, p <.01.). Overwinter' and second-year' morality
rates were not significantly different (p >0.5: 0.14 vs.

0.12 %‘day'1).

The good fit of both sets of regressions was due to very
similar patterns of mortality for all cohorts at each site

(Figure 1). These results were unexpected because, although

76

Figure 3.1 Root length survival curves for root cohorts
during 1989 and 1990. Survival times were significantly
greater at the northern site for all but the July (no
difference) and October (southern site greater) 1989
cohorts. Cohorts were comprised of all new roots present on
the minirhizotron surface that were produced between
successive sample dates in the upper 30 cm of the soil. The
data were pooled from the 12 minirhizotrons in each forest.
Each root was identified and numbered by the ROOTS image
analysis program we developed, and was remeasured and
classified as live or dead at each sampling date.
Significant differences in length survival were tested using
a Gehan-Mantel test for censored data 9 at an alpha of
0.05.

._—_,.v _/_A.; _._I___r\.lu LIP.!\ .IEl.

CZ_>_>333 .10. .00 4<ZTUB¢O no ZOCKOQOZL

PROPORTION OF ORIGINAL COHORT SURVIVING

SOUTHERN SITE

NORTHERN SITE

77

ROOT LENGTH SURVIVAL - ALL COHORTS

 

1.1
1.0

0.91
0.8-
0.7;
0.59
0.5-5
0.43
0.3;

0.24

0.1-

 

(10

 

 

 

1.1

I I r I I T I u I t I I I

7 27 17 9 29
JUNE

SEPTEMBER JANUARY MAY

 

1.0
0.9:
0.83
0.7;
0.6-
0.5-3
0.45
0.3-1
0.2;
0.11

- I Q

I ( x
\ '. ‘9’

 

---- 1990 COHORTS

 

 

989 COHORTS
1 I I I U

 

0.0

7
JUNE

T I l I I I I U I V I F

27 I 7 9 29
SEPTEMBER JANUARY MAY AUGUST

DATE OBSERVED — 1989 84 I990

78

Figure 3.2 Regressions of length mortality data against the
number of days a cohort had been under observation during
it’s first growing season, with line forced through the
origin. The slope (mortality rate) of the southern site was
significantly greater than the northern site. There were no
site differences in over-winter and second-year mortality
rates (regressions not shown). Data were pooled across all
1989 and 1990 cohorts. Differences among the two forests
were tested by comparing regression slopes at an alpha of
0.05.

79

 

 

 

 

O
O

OVECI HlONEI'I lBOHOO

_IVNIOIEIO _-IO BOVINEIDBEIcI

L
\ \ . "
\ \ ‘\ -
\ \ -
D \ \\ _
\ \‘
\ \ \ h
\ \‘ '
F'N \ \‘ C ..
C30) \ \\ _
e . ‘ \ \\ P
II II ‘9‘. A
N N \ \‘ "
0:0: ' g \ I‘ -
.. . ‘ e“ -
F“) n \ \ __
as! a ' b‘; -
\\\ "
H ” \\\ .-
V \ \ _
LLJLIJ ‘ \\\\Q _
%CCL> a ‘ "“0 .
_’._J D . . \\ b
\\\ .-
\\\ I-
HIE D \a- -
\
_ — CI Q3" \\ _
mm D H. O -
22 ‘e‘ -
(rm \\ -
LIJLIJ I \“ —
I I (“ C.
I—I— a .. “ C!
Dm L-‘; It .L'
00 'T‘ L
(DZ \
L\\\\ '-
\
IIIIIIUTTITTTTjilITITIITITTIIITIITTTIIIIIIrllillI
O O O O O O O O O O
O? (D I\ LO LO V I") (\I ‘-

180 200

4D 60 80 100 120 I40 160

20

DAYS AFTER FIRST OBSERVED

there
mortal
year,
r00t
and/o:
Keyes
1979)
refle
that
simil
bioma
produ

hard:

grgw
Grow
may

Dart
f011.

Seco

80

there have been no prior studies of differences in the
mortality rates of roots produced at different times of the
year, several studies have shown seasonal variation in fine
root turnover as calculated from temporal changes in live
and/or dead root biomass (Fogel 1983, Grier et al. 1981,
Keyes and Grier 1981, McClaugherty et al. 1982, Persson
1979). This variation is often believed to partially
reflect variable root mortality rates. However, assuming
that. the dynamics of root length and root biomass are
similar, our results suggest that temporal differences in
biomass "turnover" may be due to temporal variation in root
production, not in root mortality, at least in northern

hardwood ecosystems like the ones we studied.

Mortality rates of the 1989 cohorts were significantly less
during the winter and second growing season than during the
first growing season in both forests (Figures 1,2). Low
overwinter mortality rates might be explained by lower root
maintenance respiration rates under colder soil temperatures
(Amthor 1984, Lawrence et al. 1983, Marshall and Waring
1985), but it is unclear why roots produced in the 1989
growing season should die at a slower rate during the 1990
growing season as well. Some of the longer surviving roots
may undergo secondary growth and become a more permanent
part of the root system, but of the 2216 roots that we
followed in this study, only’ 1 developed any signs of

secondary growth. Survival of these roots may have been

enhance
cortice
resourc
answer

invest:

 

 

81

enhanced by greater lignification and/or suberization of
cortical or epidermal cells, or perhaps they were located in
resource-rich microsites. Our study was not designed to
answer these questions, but they deserve further

investigation.

The causal factors responsible for the large differences in
fine root mortality rates between these two forests are not
readily apparent. Both forests are of similar age,
structure and composition (Table 1), and there are no
substantial differences in leaf area, fertility, soil
moisture holding capacity or other site factors (MacDonald
et al. 1991, Burton et al. 1991, Pregitzer and Burton 1991)
that can be invoked as obvious explanations for the
differences in root mortality. rates and survival
distributions. It is possible that warmer soil temperatures
contribute in part to greater fine root mortality rates in
the southern forest (Table 1, Figure 3). Late-spring and
summer soil temperatures at 15 cm depth were 2-4 oC warmer
at the southern site in both 1989 and 1990. Soil
temperatures were significantly warmer at the southern site
from late April through mid-October during both years
(paired t-test; p <.001) by an average of about 1.5 C’C.
Soil temperature was not controlled in our study, and so the
evidence linking' temperature and root. mortality is
circumstantial. However, previous studies have demonstrated

increased root respiration rates and shorter root turnover

82

Figure 3.3 Weekly averages for soil temperature at 15 cm
depth at both forests. Paired t-tests of site differences
in average weekly temperatures (derived from the mean of
three sensors at each site) showed that temperatures from
26/4/89 through 17/10/89 and 30/4/90 through 16/10/90 were
significantly greater at the southern site (p <.001). Data
were collected every 30 minutes with an Omnidata monitoring
system (Omnidata International, Logan Utah, USA).

 

 

83

mmo<mm>< >I_vm_m>> cam: 8% amm—

 

 

HmDOD/x ><§ >m<DZ<e mmmfimpamm mZDp
mm m 5 mm m

_ _ L p . _ _ p _ _ _ p . _ . . . .V
wtm ZKmIHmOZ OI. I

a mtm meIHDOm _MIU o

Tm
E I

_ an TOP

 

 

 

 

 

 

 

<00) BBDIVBBdWBI "HOS

84

times associated with higher soil temperatures (Amthor 1984,
Lawrence et al. 1983, Marshall and Waring 1985), and we
believe that higher soil temperatures act in part to
accelerate mortality rates in the southern forest, probably
through greater maintenance costs throughout the entire

system of fine, absorbing roots.

Regardless of the factors responsible for the differential
rates of root. mortality that. we observed, our findings
highlight the need for a better understanding of the
processes controlling fine root inputs of carbon and
nutrients to the soil. For example, in many models of
forest ecosystem processes, the allocation and cycling of
resources belowground are driven by site factors like
nitrogen or water availability (Aber et al. 1991, Running
and Gower 1991). In others, carbon and nutrient budgets are
constructed to account for greater C costs due to increased
root respiration under warmer soil temperatures (Bonan 1991,
Ewel and Gholz 1991, Running and Gower 1991). But none that
we are aware of make allowance for differences in root
turnover rates within an ecosystem type, nor are root
turnover rates intrinsically linked empirically or directly
to soil temperature. A positive outcome from our study may
result from our observation of highly predictable mortality
rates for all roots produced within a given growing season.
If similar patterns of mortality occur in other plant

ecosystems, then it should be possible to quantify

85

belowground resource cycling in a changing environment
solely from estimates of fine root production once an
empirical relationship between soil environmental factors
and root mortality rates has been established for a given

ecosystem type.

The absence of functions and parameters describing the
heterogeneity of root turnover rates within ecosystem types
or under different soil temperature regimes should not be
equated with flaws in current models of ecosystem processes.
Instead, the incomplete nature of current models reflects
how little is known of the demographic processes (like root
mortality) that control belowground carbon and nutrient
cycling, and our poor mechanistic understanding of the
relationship between root demography and soil environmental
factors (especially temperature). Given the present level
of concern about the effects of postulated global climatic
changes on the world's forest resources, and the fact that
root systems account for substantial portion of ecosystem
carbon budgets, the continuing need for more and better data
on fine root dynamics in terrestrial ecosystems should be
apparent. Even if temperature is found to have a minimal
influence on root mortality, the fact that rates of fine
root turnover can vary substantially among virtually
identical ecosystems needs to be reconciled with current
knowledge and models of belowground processes that do not

account for this phenomenon.

86

Literature Cited

Aber, J.D., J.M. Melillo, R.J. Nadelhoffer, J. Pastor and
R.D. Boone. 1991. Factors controlling nitrogen cycling
and nitrogen saturation in northern temperate forest
ecosystems. Ecol. Appl. 1:303-315.
Author, 3.8. 1984.

The role of maintenance respiration in
plant growth. Plant, Cell Environ. 7:561-569.

Atkinson, D. 1992. How long is the span of a root? Trends in
Ecol. Evol. 7: In press.

Bonan, 6.8. 1991.

Atmosphere-biosphere exchange of carbon
dioxide in boreal forests. J. Geophys.
7312.

Res.

96:7301-
Burton,

A.J. R.G. Pregitzer and D.D. Reed. 1991. Leaf area

and foliar biomass relationships in northern hardwood

forests located along an 800 km acid deposition
gradient. For. Sci. 37:1041-1059.

Cox, T.L., l.F. Harris, 8.8. Asmus and N.T. Edwards. 1978.
The role of roots in biogeochemical cycles in an eastern

deciduous forest. Pedobiologia 18:264-271.

Ewel, K.C. and R.L. Gholz. 1991. A simulation model of the
role of ,belowground dynamics in a Florida pine

plantation. For. Sci. 37:397-438.

Fogel, R. 1983. Root turnover and productivity in coniferous
forests. Plant Soil 71:57-85.

Fogel, R. 1985.

ecosystems.

Roots as primary producers in below-ground
In: A.H.
M. Usher,

Fitter, D. Atkinson, D.J. Read and
editors.. Ecological interactions iJI soil.
Special Publication Number 4. Blackwell Scientific,

Oxford.
Gower, 8.T., H.A. Vogt and C.C. Grier. 1992. Carbon dynamics
of Rocky Mountain Douglas-fir: influence of water and
nutrient availability. Ecol. Monog. 62:43-65.

Grier, C.C.,

H.A. Vogt, M.R.
Biomass

Reyes and R.L.
distribution

Edmonds. 1981.
and above- and belowground
production in young and mature Abies amabilis zone
ecosystems of the western cascades. Can. J. For. Res.
11:155-167.

87

Harris, M.F., R.G. xinerson and N.T. Edwards. 1977.
Comparison of belowground biomass of natural deciduous
forests and loblolly pine plantations. Pedobiologia
17:369-381.

Hendrick, R.L. and R.G. Pregitzer. 1992a. The demography of
fine roots in a northern hardwood forest. Ecology
73: 1094-1104 .

Hendrick, R.L. and 3.8. Pregitzer. 1992b. Spatial variation
in tree root distribution and growth associated with
minirhizotrons. Plant Soil 143:283-288.

Joslin, J.D. and G.8. Henderson. 1987. Organic matter and
nutrients associated with fine root turnover in a white
oak stand. For. Sci. 33:330—346.

Reyes, M.R. and C.C. Grier. 1981. Above- and belowground net
production in 40 yr. old Douglas-fir stands on low and
high productivity sites. Can. J. For. Res. 11:599-605.

Lawrence, 1LT. and H.C. Oechel. 1983. Effects of soil
temperature on the carbon exchange of taiga seedlings.
I. Root respiration. Can. J. For. Res. 13:840-849.

Landsberg, J.J., M.R. Raufmann, D. Binkley, J. Isebrands and
P.G. Jarvis. 1991. Evaluating progress toward closed
forest models based on fluxes of carbon, water and
nutrients. Tree Phys. 9:1-15.

MacDonald, M.M., A,J. Burton, M.F. Jurgensen, J.M.
McLaughlin and G.D. Mroz. 1991. Variation in forest
soil properties along a Great Lakes air pollution
gradient. Soil. Sci. Soc. Am. J. 55:1709-1715.

Marshall, J.P. and R.H. Waring. 1985. Predicting fine root
production and turnover by monitoring root starch and
soil temperature. Can. J. For. Res. 15:791-800.

McClaugherty, C.A., J.D. Aber and J.M. Melillo. 1982. The
role of fine roots in the organic matter and nitrogen
budgets of two forested ecosystems. Ecology 63:1481-
1490.

Persson, H.A. 1979. Fine root production, mortality and
decomposition in forest ecosystems. Vegetatio 41:101-
109.

Pregitzer, R.G. and A.J. Burton. 1991. Sugar maple seed
production and nitrogen in litterfall. Can. J. For.
Res. 21:1148-1153.

88

Pyke, D.A. and J.M. Thompson. 1986. Statistical analysis of
survival and removal rate experiments. Ecology 67:240-
245.

Raich, J;I. and R.J. Nadelhoffer. 1989. Belowground carbon
allocation in forest ecosystems: global trends. Ecology
70:1346-1354.

Running, SJ. and S.T. Gower. 1991. FOREST-BGC, A general
model of forest ecosystem processes for regional
applications. II. Dynamic carbon allocation and
nitrogen budgets. Tree Phys. 9:147-160.

Upchurch, D.R. and J.T. Ritchie. 1983. Root observations
using a video recording system in minirhizotrons.
Agronomy Journal 75:1009-1015.

Vogt, x.a, C.C. Grier and. D.J. Vogt. 1986. Production,
turnover and nutritional dynamics of above-and
belowground detritus of world forests. Adv. Ecol. Res.
15:303-307.

CHAPTER IV

THE DYNAMICS OF FINE ROOT LENGTH, BIOMASS AND NITROGEN

CONTENT IN TWO NORTHERN HARDWOOD ECOSYSTEMS

Abstract

The dynamics of fine (<2.0 mm) roots were measured in two
sugar' maple (Age; saccharum IMarsh.)-dominated ecosystems
(Northern and Southern sites) during 1989 and 1990 using
both minirhizotrons and destructive harvests. More than 50%
of annual length production occurred before mid-summer in
both ecosystems, while the period of greatest mortality was
from late summer through winter. (About 1/3 of annual fine
root production and mortality occur simultaneously, with
little observable change in total root length pools. By
using fine root length dynamics to derive biomass production
and mortality, we calculated annual production values of
approximately 8000 and 7300 kg'ha'yr'l, respectively, at the
Southern and Northern sites, representing about 60% of total
NPP in both forests. Corresponding biomass mortality (i.e.
turnover) values were 6700 and 4800 kg'ha'yr'l, and total
nitrogen returns to the soil from fine root mortality were
72 kg'ha'yr"1 at the Southern site and 54 kg'ha'yr’l at the
Northern site. Fine roots dominated total biomass and N

litter inputs to the soil in both ecosystems, accounting for

89

90

over 55% of total biomass and nearly 50% of total N returns.
In both ecosystems, roots <0.5 mm comprised the bulk of fine
root biomass and N pools, and the contribution of these
roots to northern hardwood ecosystem carbon and nitrogen

budgets may have been underestimated in the past.

91

Introduction

Fine roots and mycorrhizae are important and dynamic
components of temperate forests. More than 50% of annual
net primary production is allocated belowground in many
forests (e.g. Fogel and Hunt 1979, Grier et a1. 1981, Harris
et al. 1977, Keyes and Grier 1981), and nutrient inputs to
the soil via fine root turnover can be as much or more than
those returned in aboveground litter (Arthur and Fahey 1992,
Cox et al. 1978, Joslin and Henderson 1987, Vogt et al.
1986a). However, the difficulties associated with studying
fine roots have resulted in a paucity of belowground data
for plant communities, and many aspects of fine root

production and mortality are still poorly understood.

One of the most frustrating problems involves quantifying
the magnitude and timing of concurrent root production and
mortality (Fogel 1985, Kurz and Kimmins 1987, Santantonio
and Grace 1987). Simulation models have shown that
production and mortality can be significantly underestimated
by failing to account for the simultaneity of both processes
(Kurz and Kimmins 1987) , and numerous computational
approaches have been devised to overcome this problem (e.g.
Joslin and Henderson 1982, McClaugherty et al. 1982).
Periodic fine root production and mortality are typically
estimated from sequential changes in live and/or dead root

mass but, unfortunately, measuring root mass or nutrient

92

content at one time renders the sampling unit useless for
further study. Not only does this add a spatial component
to sampling variability, but necessitates that production
and mortality between sampling dates be inferred by
difference, as they cannot be measured directly (Santantonio
and Grace 1987) . It has been suggested that concurrent
measurements of root decomposition rates could be combined
with root biomass data to better predict production and
mortality (Joslin and Henderson 1982, Santantonio and Grace
1987), and Joslin and Henderson (1987) used this approach to
estimate fine production and turnover in a white oak
(Qggrggg alga L.) forest. However, even when decomposition
rates are used, production or mortality estimates (although
perhaps :more accurate) are still derived. by' difference,

rather than by direct observation.4

Questions about the reliability of different approaches to
calculating root production and mortality have led to
considerable debate about the relative merits of particular
methods, as well as the accuracy of current estimates of
root production and mortality (Fairley and Alexander 1985,
Fogel 1985, Vogt et al. 1989, Singh et al. 1984, Vogt et al.
1986b). There is general agreement among scientists
studying belowground processes that there is substantial
room for improvement in root research methodology and
technology (Fogel 1990, Laurenroth et al. 1986, Raich and

Nadelhoffer 1989, Santantonio and Grace 1987, Vogt et al.

93

1989). The minirhizotron (a small observation tube inserted
in the soil) is one tool that can be used to overcome some
of the difficulties associated with techniques that rely on
solely on the physical sampling of root systems (Fogel 1990,
Hendrick and Pregitzer 1992a). Minirhizotrons provide us
with the means to study the activity of root systems over
extended periods of time in a non-destructive fashion, and
with appropriate analytical techniques they can be used to
directly measure root production and mortality independently
of one another (Hendrick and Pregitzer 1992a). The small
-size and portability of the image recording systems used
with minirhizotrons makes them ideal for field studies, and
they have been used successfully to study root growth and
mortality in both natural and agronomic ecosystems (e.g.
Cheng et al. 1990, Hansson and Andren 1987, Keng 1988,
Upchurch and Ritchie 1983, Eissenstat and Caldwell 1988,

Hendrick and Pregitzer 1992a).

Although useful for studying root dynamics, minirhizotrons
cannot be used to measure root biomass and nutrient content,
despite continuing improvements being made in both
minirhizotron technology and data analysis. Physical
properties of root systems can be measured only by taking
destructive samples of root tissue. We believe that a
combination of direct observation and destructive sampling,
capitalizing on the strengths of both approaches, can

provide a more comprehensive understanding of the fine roots

94

(Hendrick and Pregitzer 1992a).

The goals of the research described in this paper were
three-fold. First, we wanted to quantify the amount and
seasonal patterns of concurrent fine (i.e. <2.0 mm diameter)
root length production and mortality in two closely matched
sugar maple forests using minirhizotrons. Our second
objective was to use these estimates of fine root length
production and mortality to predict the dynamics of fine
root biomass and nitrogen content, and to test the accuracy
of our predictions. Our overall objective was to determine
the importance of fine roots in the carbon and nitrogen

budgets of these two forests.

Methods

Site Description

The study sites are second-growth northern hardwood forests
located in the northern lower peninsula of Michigan (Table
1) , and are separated from each other by a north-south
distance of 80 km. The two forests will be referred to as
the Southern site and Northern site throughout the paper.
Sugar maple (Age; gaggnarum Marsh.) is the dominant species
in. all structural layers of' both of’ these well-stocked

forests (Table 1) . other overstory species include red

maple (Ace; Inbrum L.), northern red oak (Quercgs rubra L.),

95

Table 4.1
study sites.

Stand, soil and climatic characteristics of the

Values are averages across plots, with

standard errors of the mean in parentheses where shown.

 

 

Seneral_§tand_gharacteristics

Latitude
Longitude
Overstory Age (yrs)
Basal Area (m 'ha'l)
Sugar Maple Basal Area (%)
Canopy Height (m)
Leaf Area Index (mz/mz)
1989
1990
Mean Annual Air Temperature (°C)
Mean Annual Precipitation 6mm)
Growing degree Days (>5.6 C)
Mean Spring - Fall Soil
Temperature (°C at 15 cm)
26/4/89 - 17/10/89
(3.5)
30/4/90 - 16/10/90

V + ' o 5

pH (1:1 Water)

Bulk Density (g'fm-3)

Nitrogen (kg'ha’ )

N Mineralization (kg'ha'l'yr'l)
Phosphorus (kg'ha' )

Organic Matter (Mg'ha'l)

Southern

EQIGSE

43°40'
86°09’
78 (5)
30 (2.0)
75 (13)
24 (1)

0.3)
0.4)

AA

14.2 (4.3)

14.6 (3.3)

4.66(.46)
1.27(.07)
1408(100)
171
156(18)
41.7(3.3)

Northern

forest

44°23'
85°50’
74 (11)
30 (2.8)
83 (5)
28 (1)

7.1 (0.9)
7.8 (0.5)
5.8
810
1944

12.9

12.9 (3.2)

4.66(.27)
1.27(.04)
1125(398)
128
191(58)

45.7(13.6)

 

96

American beech (Eagug grandifolia Ehrh.), and black cherry
(Ezgnng ggrgtina Ehrh.). The herbaceous community is
depauperate in both forests, with an average cover value of
less than 3%, and there are virtually no shrubs. The soils
at the Northern site are Alfic and Typic Haplorthods, while
those at the Southern site are Entic Haplorthods. Further
site and soil descriptions can be found in Hendrick and
Pregitzer (1992a), MacDonald et a1. (1991), Burton et al.

(1991b) and Pregitzer and Burton (1991).

Three 30 m by 30 m plots were established at each site in
1987, selected so that a maximum degree of homogeneity
existed among them with respect to physiography, soils and
vegetation (Burton et al. 1991a). In June of 1988, four
minirhizotrons (2 m long x 5.08-cm inside diameter) were
permanently installed in each plot at a 45° angle to the
soil surface to a depth of 165 on along their length (a 110
cm in vertical depth) at both sites. The portion of the
minirhizotrons extending above the soil surface was painted
and capped with a rubber stopper to prevent rainfall and
light from entering. Numbered image frames were scribed
every 1.2 cm onto the exterior surface of each minirhizotron
prior to installation so that we could return to the same
location within the minirhizotrons at all sampling dates.
The scribed image frames were oriented vertically during
minirhizotron installation. Only data from the upper 35

frames (= 30 cm vertical depth) are presented here. All

97

minirhizotron images were collected on VHS videotape with a
Circon Microvideo 9011 Color Agricultural Camera (Circon
Co., Santa Barbara CA). Each minirhizotron was imaged at
approximately 1 month intervals throughout the 1989 and 1990
growing seasons. The data presented in this paper were
collected at the Northern site on 4/27, 6/11, 6/22, 7/18,
8/18, 9/16 and 10/14 in 1989, and on 4/24, 5/23, 6/19, 7/22,
8/19, 9/19 and 10/26 in 1990. The corresponding sampling
dates at the Southern site were 4/25, 6/7, 6/21, 7/18, 8/16,
9/16 and 10/14 in 1989 and 4/25, 5/24, 6/18, 7/21, 8/18,

9/18, and 10/16 in 1990.
Fine Root Length Dynamics

An interactive PC-based software program (ROOTS) that we
have developed was used to analyze the minirhizotron video
images (Hendrick and Pregitzer 1992a, Atkinson 1992).
Beginning with images from the first sampling date at each
site, the length and diameter of all roots present in each
frame were traced using a mouse, and the measurements (in
mm) were calculated and written to a database file (dBASE
III+, Ashton-Tate, Torrance, CA) by ROOTS. The tracings of
each root were permanently saved by ROOTS on a separate disk
file. An identification code was assigned to each root and
written to the database. The code was derived from the
order in which a root was traced within an image; the frame,

minirhizotron and plot in which it was located: and the date

98

on which it was imaged. The same code (except for the
collection date) was used for each root during the analysis
of subsequent images. We were able to identify the same
roots at later dates by using ROOTS to recall and overlay
the tracings and identification code from an image at time
t-1 when analyzing time t images. Complete records were
kept for each root throughout its development, even after it

died and/or disappeared.

Each root was assigned a development stage code after it had
been traced and measured. Roots were classified as "new" if
they first appeared in an image as white in color, and
"white" at subsequent dates if they remained white or cream
in color. Roots that turned, or first appeared as, tan to
brown in color were classified as "brown". Those that
turned very dark grey or black were classified as "dead".
As roots decayed and disappeared, or disappeared without
first moving into a "dead" state, they were classified as
"missing". When all the images from a given date had been
analyzed, the database records from the four minirhizotrons
on each plot were composited into one database per plot
(Hendrick and Pregitzer 1992b). After the images from all
dates had been processed, the records for the entire year
were combined. The final database for each replicate plot
at each site was a time series of lengths, diameters and

development stages for each root.

99

To calculate monthly and annual root length production and
mortality for 1989, the white, brown and total (white +
brown) root lengths present on the April, 1989 (time t = 0)
sampling dates were summed separately for each plot. Root
length production and loss was followed until April 24,
1990. The production of new root length was calculated for
the intervals t to t+1 by summing the lengths of roots
present at time t+1 that were not present at time t, and
adding the length growth of existing roots. Mortality was
calculated by summing the length of roots that moved into
the dead or missing class during the same period, plus the
length of any roots that were dead when they first appeared
at time t+1. Percent production and mortality estimates for
the intervals between sampling dates (relative to initial
root lengths) were calculated by dividing the production and
loss of white, brown and, total root length. during the
interval by the initial (April 27, 1989) length standing
crop. Production and mortality rates for 1990 were
calculated likewise using the April 1990 length standing
crops at each site. The length data were standardized in a

length density format (mm'cm'z).
Stand Biomass and Productivity
Abgyggrgund: Tree bole and branch biomass were calculated

indirectly from measurements of diameter at breast height

(DBH) and tree height and published allometric equations for

100

each species (Monteith and Jacobs 1979, Crow and Erdmann
1983). Measurements of each tree >5 cm DBH on all plots
were made at each site in the fall of 1988 and 1989 after at
least 50% leaf fall. Net biomass increment was calculated
for the 1989 growing season as the difference between the

fall 1989 and fall 1988 living biomass.

Aboveground litterfall was measured from eight 0.5 m2 litter
traps randomly located on each plot. Material was collected
on a monthly basis from spring through late summer, and
weekly during leaf fall in the autumn. Litter samples were
air dried at 70 0C for 48 hours and weighed after they had
been sorted into foliage, reproductive (seeds, flowers,
etc.), woody and insect frass components. Litter was
composited across sampling dates on a plot basis and
analyzed for Kjeldahl N following sulfuric acid digestion
(Technicon Industrial Systems 1977). Nitrogen content was
calculated by multiplying the N concentration of each litter

component by its biomass.

Canopy leaf area index (LAI) was calculated at each site by
multiplying leaf biomass by specific leaf area (SLA). On
each litter sampling date, the area and mass of all the
leaves from one-half of each trap was determined before
drying and weighing. Species-specific LAI's were calculated
by multiplying a species litter weight by its SLA, and

canopy leaf area was then calculated by summing LAI's across

101

all species. IAI's were corroborated by allometric
equations derived from destructive harvests at each site, as
well as canopy light transmittance: further details can be

found in Burton et al. (1991).

Belowgrggng: Root biomass and nutrient content was
determined from soil cores collected on the April and
October 1989 image sampling dates at each site. Eight
cylindrical 5.08 x 30 cm biomass cores were randomly
collected from a 10 m wide border strip surrounding each
plot, and one additional core was collected within 0.5 m of
each of two randomly selected biomass core samples on each
plot for determination of root nitrogen concentrations.
Soil cores were transported on ice to the Michigan State
University campus. Roots were recovered from the soil using
an automated root washer (hydropneumatic root elutriator,
Smucker et al. 1982). The elutriator uses air bubbles to
transport organic material through a water/soil/root-filled
tube onto a 0.42 mm screen. Recovery of roots from a washed
soil sample is >99% (Smucker et al. 1987). After washing,
roots were stored at 2-3 °C in a 20% methanol solution until
they could be sorted into 3 size classes: 0.0-0.5 and 0.5-
2.0 mm (collectively termed "fine roots") and 2.0-10.0 mm.
Roots in the two largest size classes were dried at 70 °C

for 48 hrs, and weighed.

102

The biomass of roots <0.5 mm was determined indirectly.
First, total root length per sample was calculated using
Newman’s line intercept method (Newman 1966) after all roots
>0.5 mm had been removed. The grid array used for length
determination was calibrated with segments of monofilament
fishing line cut into segments ranging from 0.2-5.0 cm in
length, and in amounts proportional to those in actual root
samples. Estimated monofilament length was compared with
actual length in increments of 5.0 m, from 5.0 to 25.0 m.
The presence of many short roots/segments a few millimeters
in length resulted in a systematic underestimation of true
length, and it was necessary to multiply our initial root
length estimates by a factor of 1.59. Next, random segments
of roots 0.5 mm in diameter, totaling 50 cm in length, were
collected from each core sample after length determination.
These samples were dried as above, weighed to the nearest
0.0001 g, and average root length density (g'cm'l) ratios

for roots 0.5 mm were calculated.

The <0.5 mm root length of each sample was converted to
biomass by multiplying the length of each sample by the mean
specific root length of all 8 samples from each plot for a
given date and site. Sample biomass of both size classes
was converted to units of kg'ha'l. Root N content at each
date and site was determined by multiplying, the N
concentration of each size class (determined as for

aboveground litter) by its biomass. Biomass and N content

103

means at each site were determined from plot values derived

from the average of the 8 cores sampled on each plot.
Predicting Root Biomass Production and Mortality

Annual total fine (<2.0 mm) root production (April 1989 to
April 1990) at each site was calculated by multiplying the
initial (April 1989) biomass by the ratio of annual length
production to initial length density along the
minirhizotrons. Total biomass mortality (turnover) was
calculated similarly by multiplying initial root biomass by
the ratio of annual length mortality to initial root length
density. The amount of N allocated to new root production,
and the N lost to the soil through root death, were
calculated by multiplying initial root N content by the
length production and mortality ratios, respectively.
(These two ratios express annual production and mortality in
terms of initial conditions, and represent the proportion of
original length, biomass or N that was gained and lost

during the year.)

To check the accuracy of our estimates of root biomass and N
production and turnover, we compared the October 1989 fine
root biomass and N content data measured at each site with
predicted standing crops derived from the minirhizotron
data. Predictions of October biomass (and N content) at

each site were made by determining the amount of biomass and

104

N allocated to new roots from April to October based upon
the production of root length, and subtracting from this
value the biomass and N lost due to turnover (determined
from root length mortality) during the same period of time.
Root biomass (and N) production and mortality from April
through October were calculated in the same manner as annual
production and mortality, except April-October root length
density production and mortality values were used when
computing ratios of length production and mortality to
initial length density values. Final N content data were
adjusted to reflect the actual October N concentrations of

each size class.
Results
Fine Root Length Dynamics Along the Minirhizotrons

Fine root length density along the minirhizotrons exhibited
a unimodal pattern of increase and subsequent decline at
both sites during the 1989 and 1990 growing seasons (Figure
1) , although there were some differences among sites and
years in the timing of maximum root ‘ length densities. At
the Southern site, root length density peaked in late June
in 1989, but not until mid-July in 1990. The April-June
1989 increase was rather abrupt, and length loss was minimal
during the fall and over winter. In 1990, the increase and

decrease were both gradual. Root length densities in the

105

Figure 4.1 Total, white and brown fine root length
densities (mm root per cm minirhizotron surface) at the
Southern and Northern sites from April 1989 through October
1990. Data are plot means with standard error bars.

106

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Northern forest followed a different pattern of
developmentmaximum root length density occurred in August
1989 and mid-June in 1990. The increase and decrease in
length densities were gradual in 1989, but there was an
abrupt increase in 1990, with minimal loss through October.
Root production was greater than mortality for the one year
period from April 1989 to April 1990 at both sites (Table
2), resulting in net increases inApril 1990 length (Figure
1). At the Southern site, relatively greater mortality
during 1990 resulted in October 1990 length densities that
were not significantly different from April 1990 values (t-
test, alpha = .05) ). However, length density at the

Northern site continued to increase during 1990 as well.

The composition of root length, with respect to white and
brown roots, was greatly different among the sites (Figure
1). In the Southern forest, white roots comprised 32 to 55%
of total root length throughout the study period, but only
10 to 41% of total root length at the Northern site. The
difference in length composition is due to site differences
in mortality rates of the newer white and older brown roots.
Equal amounts of white and brown root length contributed to
total mortality at the Southern site (Table 2), while nearly
3/4 of root length mortality in the Northern forest was due
to the death of brown roots. White roots were most abundant
in the late spring and early summer at both sites during

1989 and 1990 (Figure 1).

108

Table 4.2 Site means (and standard errors) of initial root
length density, annual length production and annual
mortality (April 1989 to April 1990).

 

 

Southern Site Northern Site
Initial Length
Density (mm'cm’z) 3.34 (.08) 3.60 (.26)
Total Annual
Length Eroduftion
(mm'cm' 'yr' ) 3.38 (.61) 3.83 (.50)
Total Annual
Length Mortality
(mm'cm' ‘yr' ) 2.82 (.38) 2.56 (.57)
White Length
Mortality
(% Total) 50.5 (13) 25.4 (3)

Brown Length
Mortality
(% Total) 49.5 (13) 74.6 (3)

 

109

Figure 4.2 Percentage distribution of total growing season
(April-October) fine root production and mortality occurring
between minirhizotron sampling dates. April/May and
May/June data in 1989 were calculated from April-early June
and early June-late June data by interpolation, assuming
that production and mortality were evenly distributed during
the 6 week interval from late April to Early June at both
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There were distinct seasonal patterns of root length
production and mortality during the 1989 and 1990 growing
seasons (April - October) at both sites (Figure 2).
Although a significant amount of both production and
mortality occurred simultaneously, more than 50% of total
growing-season production took place between late April and
mid-to-late July. Patterns of length production were
similar both years at the Southern site, at the Northern
site but there was a distinct peak in production during the
1990 May/June interval (Figure 2). The effect of this
sudden burst of production is evident as an abrupt increase
in root length density at this site during the same period

of time (Figure 1).

The greatest amount of root mortality occurred after mid-
summer, although relative amounts of root mortality varied
somewhat within and between years. There was a large die-
off of root length during the August/September 1990 interval
at the Southern site, the effects of which are manifested in
total root length density (Figure 1) . Expressed on an
annual basis (April 1989 to April 1990) it is apparent that
over winter losses of root length contribute a much greater
amount to total root mortality at the Northern site (Figure
3). Only 25% of total annual root mortality occurred during
the six month interval from October 1989 to April 1990 at
the Southern site, but nearly 40% of total annual root

length mortality took place during the same period of time

112

Figure 4.3 Percentage distribution of annual (April 1989 -
April 1990) fine root production and mortality occurring
between minirhizotron sampling dates.

113

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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in the more northern forest.

Fall and over winter root production contributed little to
total annual production at either site (Figure 3). From 85
to 90% of all root length ‘was produced prior to mid-
September at both sites (Figure 4), and over winter
production contributed only 7% to the total. The greatest
amount of production occurred from late April to June, also
the period in which budburst occurs (early-to-mid May) and
canopy leaf expansion reaches 100% (late May to early June)

in both forests (unpublished data).

The asynchrony of maximum relative root birth and death
rates results in a distinct lag between cumulative length
production and mortality (Figure 4) . The two-week period
between the mid and late-June 1989 observations was that in
which the most rapid divergence of production and mortality
occurred at both sites. The lag between production and
mortality was greatest at the Northern site, due to
relatively less root length mortality during the growing
season. The greater lag between the production and
mortality curves, and the lower annual root length mortality
at the Northern site (Table 2) suggest that fine roots are
living longer in this forest. Indeed, survival analyses of
root cohorts born during the intervals between observations
show that fine roots in the Southern forest consistently die

at rate 64% greater ‘than roots in the Northern forest

115

Figure 4.4 Cumulative (%) fine root production and
mortality at the Southern and Northern study sites.

The
horizontal distance between the two curves at each site is a
relative index of turnover time.

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(unpublished data).
Pin. Root Biomass and Nitrogen Content

Patterns of biomass distribution among the three size
classes of roots were similar at both sites and on both
sampling dates (Table 3). There was a considerable amount
of mass in the smallest class of roots (<0.5 mm): about
6,000 kg'ha'1 at the Southern site and 5,500 kg'ha'1 at the
Northern site. In fact, the April <0.5 mm fine root biomass
was nearly equal in magnitude to the combined mass of the
two other size classes. However, there was a considerable
(though not statistically significant) biomass increase in
the largest size class (2.0-10.0 mm) by October, so that the
masses of the smallest and largest classes were nearly equal
(Table 3). The least amount of biomass was in the
intermediate (0.5-2.0 mm) class of roots at both sites and
on both sampling dates; about 1/3 that of the smallest roots
in the spring and about 1/2 the mass of the smallest roots
in the fall. The intermediate class increased significantly
(t-test, alpha 8 0.5) in biomass from April to October, but
there were virtually no seasonal differences in the mass of

the smallest roots.

The biomass of the smallest roots (<0.5 mm) was greatest at
the Southern site on both dates, but differences among sites

were statistically significant only in April (t-test, alpha

2» my 20 mo

mo

118

Table 4.3 Biomass and nitrogen content (kg'ha'l) of roots
<0.5, 0.5 to 2.0 and 2.0 to 10.0 mm in diameter, as
determined from soil cores. Plot means with standard errors
in parentheses.

 

 

Southern site

 

<0.5 0.5 - 2.0 2.0 - 10.0
April 1989
Biomass 6110 (97) 1791 (84) 5389 (599)
April 1989
N Content 70 (2) 15 (l) 28 (5)
October 1989
Biomass 6249 (352) 3281 (153) 6550 (662)
October 1989
N Content 73 (7) 26 (1) 27 (5)

Northern Bite

 

(0.5 935 - 200 200 - 4000
April 1989
Biomass 5413 (46) 1474 (79) 3377 (103)
April 1989
N Content 72 (1) 13 (1) 17 (1)
October 1989
Biomass 5553 (422) 2414 (78) 5392 (1442)

October 1989
N Content 52 (4) 16 (1) 29 (8)

 

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119

= 0.05). The mass of the other size classes was
consistently greater at the Southern site as well, but the
only statistically significant difference in addition to
that described above was for the 0.5-2.0 size class in
October. The combined April and October biomass of the two
smallest classes of roots was, respectively, 7901 and 9530
kg'ha-1 at the Southern site and 6913 and 7967 kg'ha'1 at

the Northern site.

Patterns of root N content were similar to those for
biomass. At each site, the greatest amount of N was found
in roots <0.5 mm in diameter on both sampling dates.
Differences in N content between the two largest size
classes tended to be less pronounced than biomass
differences because of higher N concentrations in the 0.5-
2.0 mm roots (Table 4). There was no difference between the
April and October N content of smallest roots at the
Southern site. However, there was a substantial drop in the
N content of these roots at the Northern site, due to a 25%
decrease in N concentration (Table 4). Among the two
largest size classes, only the N content of 0.5-2.0 mm roots
at the Southern site changed significantly (t-test, alpha =
0.05) from April to October. In contrast to the smallest
roots at the Northern site, the temporal difference in the N
content of this class was due to a change in biomass, not
concentration (Table 4) . There was a substantial, though

not statistically significant (alpha = .05), increase in the

120

Table 4.4 Nitrogen concentration (%) of roots <0.5, 0.5 to
2.0 and 2.0 to 10.0 mm in diameter. Plot means with
standard errors in parentheses.

 

 

southern site

<0. gsfi-zgg . - .
April 1989 1.15 0.84 0.51
October 1989 1.16 0.79 0.41

Northern site

(0:: 905-239 - .0
April 1989 1.33 0.88 0.51

October 1989 0.93 0.66 0.54

 

0:

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TI

121

October N content of the largest roots at the Northern site,
again due to a change in biomass and not N concentration.
There were no consistent site differences in N contents of
the two largest classes of roots, but they tended to be
higher at the Southern site. At the April sampling date,
only the N content of the largest roots was significantly
different (t-test, alpha = 0.05) among the sites, while in
October both the smallest (alpha = .10) and intermediate

(alpha = 0.05) size classes at the Southern site had more N.

Root Production, Mortality and standing Crop Predictions

At both sites, predicted fine (<2.0 mm) root production for
the period April 1989 to April 1990 was greater than
predicted mortality (Table 5) . Predicted production and
mortality at the Southern site were approximately 8,000 and
6,700 kg'ha-l'yr'l, respectively. The corresponding values
at the Northern site were 7,300 and 4,800 kg'ha'l'yr'l.
Total N allocated to new roots (i.e. production) was nearly
the same at both sites (85 and 86 kg'ha'l'yr'l) despite the

nearly 800 kg'ha"1 '

yr'l difference in biomass production.
This was due largely to the higher N concentration of roots
in April at the Northern site (Table 4). Total N returns to
the soil via root mortality were estimated 72 and 54 kg'ha'

1'yr'1 at the Southern and Northern sites, respectively.

122

Table 4.5 Comparison of measured and predicted 1989 total
fine (0.0-2.0 mm) root biomass and nitrogen content standing
crops, and predicted annual (April 1989 - April 1990)
production (and. mortality; ‘Values are in. kg'ha' , with
standard errors in parentheses.

 

 

Southern site Northern Bite

mm W 2133195

April

Biomass 7901 (76) 6887 (192)

Annual

Biomass

Production 8081 (1619) 7302 (663)

Annual
Biomass
Mortality 6682 (892) 4843 (929)

October
Biomass 9530 (555) 10299 (757) 7968 (866) 10708 (514)

April N
Content 86 (1) 85 (2)

Annual N
Production 87 (17) 88 (8)

Annual N
Mortality 72 (9) 54 (9)

October N
Content 99 (7) 106 (7) 68 (8) 91 (4)

 

123

Our predictions of October fine root biomass and N standing
crops (i.e. measured April standing crops + estimated April
to October production less estimated April to October
mortality) varied among the two sites in their accuracy.
Our estimate of an October biomass standing crop of 10,299
kg'ha'l at the Southern site was 8.1% greater than the
measured standing crop of 9530 kg‘ha"1 (Table 5), but the
two values were not significantly different (alpha = 0.05).
Similarly, the estimate of an October N content of 106
kg'ha'l was 7.1 % greater than the measured value of 99
kg'ha'l, and. again. not statistically' different (alpha, =
0.05) . However the predicted and measured biomass and N
standing crops were substantially different at the Northern
site. The predicted October biomass standing crop was 34.4%
greater than the measured value (10,708 gs. 7,968 kg'ha'l),
and the predicted N content of the roots was 33.8 % greater
than the measured value (91 gs; 68 kg'ha‘l). Both
differences were statistically significant (t-test, alpha =

0.05)‘

Above- and Belowground Standing Crops, Production and

Litterfall

Aboveground woody biomass was greatest at the Northern site
(Table 6); 277,300 kg'ha'1 gs. 236,200 kg'ha'1 at the
Southern site. Foliage biomass was just over 4,000 kg'ha'1

at both sites, and not significantly different among the

124

Table 4.6 Above- and belowground (less coarse roots >10 mm)

April 1989 biomass, in kg'ha' .
errors in parentheses.

Plot

means with standard

 

 

Southern_§its

Aboveground
Woody 236,200 (17,300)
Foliage 4,225 (412)
Roots (in mm)

2.0-10.0 5,389 (599)

0.5-2.0 1,791 (84)

0.0-0.5 6,110 (97)
Total 253,715

Northern_§ite

277,300 (17,600)

4,068 (357)

3,377 (103)
1,474 (79)
5,413 (46)

291,632

 

sites
13,2!
the
stan
both
folf
Sou‘
sit
ref
for

trx

To‘
in
at
di

We

125

sites (Burton 1991b). Total biomass of roots <10.0 mm was
13,290 kg'ha"1 at the Southern site and 10,264 kg'ha"l at
the Northern site. Expressed as a percentage of total
standing crop, biomass distribution was nearly the same at
both sites. Aboveground woody biomass accounted for 93.1%,
foliage 1.7% and roots 5.2% of total standing crop at the
Southern site. The corresponding values at the Northern
site were 95.1, 1.4 and 3.5%. Of course these values do not
reflect the actual total distribution of biomass in these
forests, as the mass of roots >10.0 mm (often roughly 20% of

true total standing crop) was not determined.

Total above and belowground NPP (less the coarse root
increment) was nearly equal at both sites (Table 7), with
about 7% more production at the Southern site. The
distribution of NPP among the three components we measured
was also the same at both sites. Only about 10% of NPP was
allocated to the production of bolewood and branches (1,222
and 1,233 kg'ha‘yr'l at the Southern and Northern sites,
respectively). Foliage production accounted for 30% of NPP,

while about 60% was allocated belowground to roots <2.0 mm.

Leaf litterfall and fine (<2.0 mm) root turnover dominated
carbon and N inputs to the forest floor and soil (Table 8).
Leaf litter accounted for 35% of total above- and
belowground litter biomass at the Southern site, and just

over 40% at the Northern site. Most of the remaining litter

(NF
Apr
NPE

Fo
Ro

T0

126

Table 4.7 Abovi- an? belowground net primary production
(NPP), in kg'ha- 'yr' , for the period April 1989 through
April 1990. Data are plot means, with percentage of total
NPP in parentheses.

 

 

Seutbsrn.§its Herthsrn_§it§
Aboveground
Woody 1,222 (9) 1,233 (10)
Foliage 4,225 (31) 4,068 (32)
Roots <2.0 8,081 (60) 7,302 (58)

Total 13,528 12,603

 

127

Table 4.8 Above- and belowground litter biomass and N
returns to the soil from Apral 1989 to April 1990. Data are

expressed in units of kg'ha' , and as a percentage of total

 

 

litterfall. Plot means with standard errors in parentheses.
Southern Site
Bi9msss 1.19191 11119999 1.19191
Foliage 4225 (412) 35.1 36.7 (5.7) 29.5
Reproductive 622 (115) 5.1 12.6 (3.7) 10.1
Woody 514 (101) 4.3 2.9 (0.5) 2.3
Root <2.0mm 6682 (892) 55.5 72.3 (9.3) 58.1
Total 12,043 124.5
Northern Site
Bi9msss 1.19191 N11r9ssn 1.19191
Foliage 4068 (357) 40.8 38.7 (1.8) 35.2
Reproductive 715 (181) 7.2 15.9 (4.1) 14.5
Woody 348 (126) 3.5 2.3 (0.7) 2.1
Root (2.0mm 4843 (929) 48.6 53.1 (8.6) 48.3
Total 9,974 110.0

 

in;
505
brz
re
f o
k9

I'E

128

input at both sites was due to fine root turnover (around
50%) . The total contribution of reproductive and small
branch litter was about 10% at both sites. Patterns of N
return were similar, although reproductive litter accounted
for over 10% of total N returns by itself (12.6 and 15.9
kg'ha'yr"1 at the Southern and Northern sites,
respectively). The amount of N in leaf litter was 36.7
kg'ha'yr'l at the Southern site and 38.7 kg'ha'yr'l at the
Northern site. The corresponding values for root N inputs

were 72.3 and 53.1 kg'ha'yr'l.
Discussion

We observed a unimodal seasonal pattern of fine root length
densities during 1989 at both sites, and there appears to be
a large degree of both temporal and spatial consistency in
the cycles of fine root length gains and losses in these
northern hardwood ecosystems. This pattern of root length
increase and decline may be linked to phenological and
physiological events in the canopy. There is a substantial
increase in root length as the canopy flushes in late
spring, and maximum amounts of root length occur in mid-
summer when evaporative demand is high and soil water is
typically at relatively low levels in these forests. Fine
root length subsequently declines around the onset of canopy
senescence and leafall. The summer maximum in root length

that we observed is in general agreement with the trends

bio
198

198

Sea
lit
mor
eff
dis
pea
pro
Kur
198
def
bio
Per
Nev
bio
dif
Cal
Kim
Pro
Una.
tHr:
in .

bet‘

129

biomass data from some other deciduous (Joslin and Henderson
1987, McClaugherty et al. 1982) and coniferous (Gholz et a1.
1986, Nadelhoffer et al. 1985) forests in eastern North

America.

Seasonal patterns of fine root length densities reveal
little about the dynamics of fine root production and
mortality, as changes in root length reflect only the net
effect of these two processes. There has been much
discussion in the literature regarding the need to identify
peaks and troughs in seasonal fine root biomass so that
production and turnover can be accurately measured (e.g.
Kurz and Kimmins 1987, McClaugherty et al. 1982, Vogt et al.
1989, and there has been even more discussion as to the
definition of "real" temporal increments and decrements in
biomass (Fairley and Alexander 1985, Laurenroth et al. 1986,
Persson 1978, Singh et al. 1984, Vogt et al. 1986).
Nevertheless, neither the identification of fine root
biomass minima and maxima, nor significant temporal
differences in standing crops, is sufficient to accurately
calculate fine root production and mortality. Kurz and
Kimmins (1987) demonstrated that calculating fine root
production from changes in root biomass can result in large
underestimates of actual belowground productivity and
turnover if root production and mortality are co-occurring
in time. And, the greater the degree of temporal synchrony

between production and 'mortality, the greater the

130

underestimation of either process.

The fine root minirhizotron data obtained from our study
sites consistently show a large amount of concurrent
production and mortality; much more than could be calculated
solely from changes in live or dead root mass. Although the
majority of fine root production occurs in the spring, and
the bulk of mortality in the fall and winter (Figures 2 and
3), both processes are nearly equal in magnitude during the
summer. Total fine root length changes relatively little
during this time (Figure 1), but over 1/3 of annual
production occurs between June and September at both sites,
and approximately 40% and 30% of annual mortality occurs
during the same period of time at the Southern and Northern
sites, respectively. Clearly, any physical sampling scheme
or accounting procedure that relies solely on changes in
root biomass (live or dead) to calculate production and
turnover will result in considerable underestimates of true
values in these forests. The measurement of fine root decay
rates should increase the accuracy of root production and
turnover estimates if live and dead roots can be separated
consistently. However, we have shown that fine roots in
these forests generally disappear much more rapidly than
buried-bag decomposition data would suggest (Hendrick and
Pregitzer 1992a). Fine roots are no longer visible in the
minirhizotrons within a month or so after death, similar to

the disappearance rates observed by Rogers (1939) for apple

r0
rc
tr

1::

131

roots. The absence of an accumulating pool of dead roots or
root-derived detritus in these and other forests suggests
that current estimates of fine root decomposition rates are

too low (Fahey 1992), and in need of further study.

A notable difference between the two forests we studied is
in the balance of white and brown root length observed
throughout ‘the year, and the contribution of 'these two
classes of roots to total root turnover (Table 2). Although
all roots are white when first produced, there is always a
higher proportion of brown' root length visible in the
minirhizotrons at the Northern site. We have previously
shown that white roots in this forest are consistently more
likely to turn brown rather than die throughout the year
(Hendrick and Pregitzer, 1992a). Conversely, white roots at
the Southern site are equally (or more) likely to die than
to turn brown from one sampling date to the next
(unpublished data). As the mortality data from this study
show (Table 2) , a much higher proportion of total root
length mortality is comprised of white roots at the Southern
site, with white and brown roots contributing equally to
total length turnover. A lower proportion of standing white
root length at the Northern forest may have important
implications for nutrient uptake capacity, as the brown
roots probably lose much of their ability to actively take
up nutrients via symplastic pathways once the living tissue
of their cortex is shed.

The

fal

br=

1e

10

pr

to

(G

a\

a}

a4

132

The autumnal decline in the N concentrations of roots <2.0
mm at the Northern site is partially a result of spring vs.
fall differences in the relative abundance of white and
brown roots (Figure 3). While roughly 1/3 of all root
length was white in color in April 1989, only a little over
10% was white in October of the same year. We have
previously shown that the white roots of sugar maple in this
forest lose about 40% of their N as they turn brown
(Goldfarb et al. 1990), and we attribute the October drop in
average N concentration from 1.33 to 0.93% to the greater
abundance of brown roots in the fall. The fact that the
proportions of white and brown roots remained fairly stable
at the Southern site is probably responsible for the

constant N concentration in fine roots at this site.

Our estimates of total fine (<2.0 mm) root biomass are
generally greater than those reported from other North
American deciduous forests (Table 9). Our values are
reasonably close to Powell and Day’s (1991) estimate of 7430
kg'ha'1 for roots <2.0 mm in a mixed hardwood forest in the
Great Dismal Swamp, and to Cox et al.’s (1978) report of
8500 kg'ha'lfor roots <5.0 mm in a “1192111913211 W
stand. There are fewer N content data for comparison but
again, with the exception of Cox et al. (1978) our estimates
are considerably higher than other published values. Fine

roots <0.5 mm accounted for the bulk of the <2.0 mm root

ReI

Su

133

Table 4.9 Comparison of fine root biomass and nitrogen
standing crops and annual production in some North American

deciduous forests. Biomass and N standing crap and
production values are in units of kg'ha' and kg'ha ‘yr' ,
respectively.

 

 

Standing Crop Production
191991.129; 1.191199 1! 21911919 1 19:91:19.9
Sugar maple 4280 50 4020 47 Nadelhoffer
et al. 1985
Red oak/maple 5100 57 4900 73 McClaugherty
9900 184 et a1. 1982
Sugar maple 3230 6500 Aber et al.
1060 1985
White oak 4120 48 850 10 Joslin and
Henderson
1987
Tulip poplar 8500 96 6750 76 Cox et al.
1978
Oak, gum, 7430 9890 Powell and
maple 3450 Day 1991
Sugar maple 7901 85 8081 87 This study
6887 85 7302 88

 

mass
than
are
and
<0.5
thar

root

film
to

ove
bic
our

the

We

1a

re

11:

III

134

mass and nutrient content in the forests we studied (greater
than 70% of root mass and total‘N is in these roots), and
are largely responsible for the disparity between our data
and other reports. In fact, the biomass and N values of the
<0.5 mm roots in our forests (Table 3) are equal or greater
than most other investigator’s estimates of the mass for all
roots <2.0 or 3.0 mm. We estimated the mass of roots <0.5
mm indirectly (by converting length to mass), and there is
always a degree of uncertainty when using an indirect method
to estimate an ecosystem component. It is possible that we
overestimated total root length before converting to
biomass, but we believe not. We incrementally calibrated
our procedure against known lengths of monofilament line

that bracketed the lengths estimated from our core samples.

We believe that a better recovery of the very fine roots,
largely due to the mechanical root washing system we used,
is responsible for most of the differences between our
results and those of other investigators. The
hydropneumatic elutriation system (Smucker et a1. 1982) uses
air bubbles and water to separate roots from soil, and to
subsequently gently deposit the roots on a 0.4 mm mesh
screen. In other studies (e.g. Joslin and Henderson 1987,
Nadelhoffer et al. 1985, Powell and Day 1991), fine roots
have been recovered by washing soil samples through fine
screens with mesh openings equal to or greater than 0.5 mm

(as much as 2.0 mm) in size, or by a combination of hand

135

Figure 4.5 Cumulative diameter distribution of fine root
length and numbers at both study sites on the July 1989
sampling date. Data represent values summed across all
plots: 587 roots and 3262 mm of root at the Southern site,

with corresponding values of 662 and 4059 at the Northern
site.

HI IMHTR“,

(“I lMl II A I I\_/I'

CUMULAHVEINUMBERS

CU MULATIVE LENGTH

136

 

1.0
0.8—

0.65

 

 

 

 

 

0.4-3

0.2—

0.0-
0.0 0.1

 

———-‘
GI."

/ --— NORTHERN
/ -—— SOUTHERN

”WW“..- -....-W, r
0.2 0.3 0.4 0.5 0.6 0.7 0:8 019 1.0
ROOT DIAMETER (IN MM)

 

137

sorting and sieving (McClaugherty et a1. 1982). Our
minirhizotron data indicate that at least 80% of all roots
at our study sites are <0.5 mm in diameter (Hendrick and
Pregitzer 1992a, Figure 5), and it is likely that we would
have missed many of these roots if we had washed our samples
by hand through a larger screen. Although some of these
very small roots may remain attached to larger roots during
hand washing, in our elutriated samples almost all roots of
this size are detached. The number of these small, delicate
roots in a soil core sample is staggering, and they would be
virtually impossible to recover by hand. The fact that the
percentages of total root length (80%) and numbers (ca. 85%)
comprised of roots <o.5 mm (as observed in the
minirhizotrons, Figure 5)) are similar to the percentage of
total root biomass (>70%) accounted for by roots <0.5 mm in
diameter gives us further confidence that our biomass
estimates are reasonably accurate. Visual inspection of the
graphical data of’ McClaugherty et. a1. (1982), who hand
sorted their roots into size classes, shows that the mass of
roots <0.5 represented about 1/2 to 2/3 of the total mass of
all roots <3.0 mm in the organic layer of the soil. These
proportions are not greatly different from ours, given the
wider diameter class they used, although their data for
mineral soil horizons indicates a more equal distribution of
biomass among the size classes. It is our belief that the
contribution of the very finest roots (ca. <0.5 mm) to total

root system biomass and nutrient content has probably been

138

underestimated to some extent in some past studies. This
might be especially true in forests dominated by deciduous
trees, where fine non-woody roots generally have small
average diameters (Fahey et al. 1988, Goldfarb et a1. 1990,
Pregitzer et al 1990) and where many species (like sugar
maple) form ‘vesicular-arbuscular' mycorrhizal (VAM) roots
that. are more easily' broken. during handling than

ectomycorrhizal roots.

We observed a substantial (although not statistically
significant) April-to-October increase in the biomass of
roots >2.0. mm at both sites (Table 3) that may be have been
due to an autumnal loading of storage carbohydrates, rather
than an increase in structural biomass. Starch levels in
sugar maple roots reach minimal levels in late spring after
budbreak (Wargo 1979), begin increasing in July, and reach a
maximum in late fall (Wargo 1971). Carbon is allocated
preferentially to storage carbohydrates, rather than to
radial growth in the coarse roots of sugar maple, and little
growth occurs until after leaf fall (Wargo 1979). Similar
patterns of carbohydrate deposition in roots have been shown
for other deciduous species including red (Q. Ma) and
white (Q. alga) oak (Wargo 1976), hybrid poplar (Nguyen et
al. 1990), and turkey (Q. 1mg Walt.) and bluejack (Q.
inggng Bartr.) oak (Woods et al. 1959). ‘

139

As was true for standing crops, our estimates of fine root
biomass and N production and turnover (Tables 5 and 9) are
greater than many published values. However, relative to
initial or average standing crops, our estimates are in
general agreement with many others. Annual (April-April)
biomass and N allocation to fine root production was just
slightly greater than the April standing crops, and Cox et
al. (1978), McClaugherty et al. (1982), Nadelhoffer et al.
(1985) and Powell and Day (1991) also report annual
production estimates that are very similar to standing crop
values. The annual production data of Aber et al. (1985)
from a sugar maple stand in Wisconsin range from about 33 to
200% of standing crop, depending on the method of
calculation used, while Joslin and Henderson (1987)
estimated that annual production Of roots <2.0 mm is only
about 20% of standing“ cropv (Table 9). 'The similarity
between our production data (expressed as a percentage of
initial standing crop) and those of other investigators
leads us to believe that the absolute differences in
production, like standing crop, are again due to a greater
amount of very fine (ca. <0.5 mm) roots measured in our

forests than in other ecosystems.

With respect to total (above- and belwoground) stand
biomass, fine roots ((2.0 mm) represented a relatively small
proportion in both of the forests we studied: 3.1% of total

biomass (less coarse roots >10.0 mm) at the Southern site

140

and 2.4% at the Northern site (Table 6). Similar values
have been found by numerous other researchers in a wide
array of forests types (Arthur and Fahey 1991, Fogel and
Hunt 1979, Gower et al. 1992, Grier et al. 1981, Keyes and
Grier 1981). However, as has also been observed in a number
of forest types, a substantial proportion of annual net
primary production, about 60%, is allocated to fine roots in
the ecosystems we examined. Fine root production is roughly
twice foliage production, and six times bole and branch
production, in both forests. Fine root ((2.0 mm) turnover
also dominated carbon and nutrient inputs to the soil,
accounting for approximately 56 and 49% of total) C, and 58
and 48% of N cycled annually at the Southern and Northern

sites, respectively.

Our estimates of the contribution of fine roots to stand NPP
(Table 8) are considerably higher than those of Nadelhoffer
et al. (30%, 1985) and Aber et al. (41%, 1985) for sugar
maple forests in Wisconsin. It should be noted, however,
that our estimates of aboveground standing crop and leaf
area are also greater than these Wisconsin forests.
Nadelhoffer and Raich (1992) have recently suggested that
fine root production may be positively correlated with
aboveground productivity. Greater total stand biomass and
productivity in the forests we studied may also reflect a
longer growing season or more moderate climate on the

leeward side of Lake Michigan. Our fine root data are

141

comparable to those of Cox et al. (1978), who estimated that
fine root death and decay accounted for 67% of biomass
litter production and about 60% of N cycled via detritus in
a tulip poplar stand. And, although higher than the
estimates of Reyes and Grier (1981), Gower et al. (1992) and
Arthur and Fahey (1992), our production and turnover values
are similar to some of the data from western coniferous
forests. Grier et al. (1981) estimated that 55% of total
ecosystem NPP was allocated to fine roots in a 23 year old
Pacific silver fir stand in Washington, while the
corresponding value from a 180 year old site was nearly 69%.
Fogel and Hunt (1983) estimated that about 73% of NPP is
allocated to fine roots and mycorrhizae, and that fine root
and mycorrhizal turnover was responsible for about 85% of

all detrital N inputs, in an Oregon Douglas-fir forest.

One of the reasons that the 1989 fine root allocation and
litter return percentages in our forests were so high was
because stem and branch production was quite low relative to
other years. Annual bole and branch biomass production was
just over 1,200 kg'ha'1°yr'1 in both forests during 1989,
while 1990 production was 6,000 and 5,500 kg’ha":"°yr'1 in
1990 at the Southern and Northern sites, respectively. We
suspect that the low amount of aboveground production in
1989 may have been a residual effect from the 1988 drought.
Also, fine root growth is inhibited and turnover rates are

accelerated at low levels of soil moisture availability

142

(e.g. Bartsch 1987, Kuhns et al. 1985, Rogers 1939,
Santantonio 1982), and it is likely that a large amount of
root production occurred in 1989 as absorbing area was re-
established in these forests. The effects of substantial
root production on total ecosystem productivity would be
likely to show up as reduced stemwood production, since fine
roots are a higher C allocation priority (Waring and Pitman
1985) . Pregitzer and Burton (1991) demonstrated a direct
tradeoff between the production of foliage and reproductive
litter in the forests, and similar tradeoffs in whole-tree
carbon allocation may be occurring with respect to fine root

and bolewood production.

In the forests we studied, more C and N was cycled via fine
root turnover than abovegroundi litterfall. The same
phenomenon has been observed in a number of forests
worldwide (Vogt et al. 1986a) , and comparative data from
other studies suggests that fine root production surpasses
foliage production in most deciduous forests of the eastern
0.8. (Table 10). The ratio of root production to total
foliage biomass at both of our study sites is close to the
value of 1.92 derived by Raich and Nadelhoffer (1989) for
the ratio of aboveground litterfall carbon to total root
carbon allocation, although they included root respiration
in addition to biomass production. Our data fall somewhere
in the middle of the range of values we derived from other

ecosystem studies, including the sugar maple stands studied

143

Table 4.10 Annual fine root production per unit leaf weight
and leaf area in some temperate North American deciduous
forests. Leaf biomass data were derived from published
estimates of leaf litter production.

 

 

kg Root/ k Root/

W 131.1511: _Leaf Reference

Sugar Maple 1.40a ---- Nadelhoffer et
al. 1985 F“

Sugar Maple 3.10a ---- Pastor et al.
1984, Aber et
al. 1985

Oak-Red Maple 1.23b ---- McClaugherty et
al. 1982

White Oak 0.26c ---- Joslin &
Henderson 1987

Tulip poplar 2.04d 0.095 Cannell 1982,
Cox et al.
1978

Sugar Maple 1.91 0.10 This Study

(Southern)

Sugar Maple 1.79 0.10 This Study

(Northern)

 

a production calculated by difference using nitrogen
budgeting technique

b production calculated as difference of minimum and maximum
annual root mass

c production calculated by balancing production, mortality
and decomposition

d production calculated as root death/decay data

144

by Nadelhoffer et al. (1985) and Aber et al. (1985). Our
data are quite similar to the value of 2.04 for the tulip
poplar stand of Cox et al. (1978). Perhaps of even more
functional significance is the relationship between leaf
area and fine root production. Even though there were some
site differences in both leaf area (Table l) and root
production (Table 5), the ratio of root mass production to
leaf area was the same in both forests. Unfortunately,
there are ‘very’ few other' published data from. deciduous
forests for comparison, but our estimates are again nearly
the same as to that derived from the data of Cox et al.

(1978) and Cannell (1982).

The validity of our estimates of the role of fine roots in
ecosystem processes in these forests is dependant upon the
accuracy of our estimates of root production and mortality.
We calculated April 1989 to April 1990, and April-October
1989, production as being greater than concurrent mortality
during the corresponding periods of time in both forests.
Consequently, we predicted that the October 1989 standing
crops should be greater than the April values.
Encouragingly, the October 1989 increase in biomass standing
crops (Table 5) indicates that the increases in root length
that we observed with the minirhizotrons during the growing
season were real and reflected corresponding changes in
biomass. However, the accuracy with which we were able to

predict fine root production and mortality, and changes in

 

145

standing crops, from the biomass and minirhizotron data are
somewhat mixed. Based upon the close agreement (not
significantly different at alpha = .05) between actual and
predicted October biomass and N standing crops, we appear to
have predicted biomass and N production and mortality fairly
closely at the Southern site, and we have a high degree of
confidence in our estimates for this site. However, we
overestimated October biomass and N content at the Northern
site by about 34%, indicating that either our production
estimates for this site are too high, our estimates of April
or October fine root biomass are incorect, or our mortality
estimates are too low. It is our opinion, that the
discrepancy between the actual and predicted October 1989
biomass values at the Northern site is due primarily to an
underestimate of root mortality, and to a lesser degree an

overestimate of root production.

The reasoning for this statement lies in our belief that
root length and age distributions had probably not
equilibrated along the minirhizotron surface when we began
imaging in 1989. These forests experienced a 50 yr drought
in 1988. Because root growth is inhibited (Deans 1979,
Kaufmann 1977, Kuhns et al. 1985, Taylor and Davies 1990,
Teskey and Hinckley 1981) and root aging (i.e.
"suberization") and turnover rates are accelerated (Bartsch
1987, Kuhns et al. 1985, Rogers 1939, Santantonio 1982) at

low soil moisture potentials, new root growth was probably

E

146

comparatively low during most of the 1988 growing season and
root mortality rates may have been rather high. As a
result, the initial root length densities along the
minirhizotron surface may have been somewhat lower than they
would have been had we had normal amounts of precipitation
in 1988, and age distributions would have been skewed
towards younger roots. Because production and mortality
rates were derived as a proportion of initial root length
densities, actual production would have been overestimated,
and root mortality underestimated. A bias towards younger
roots would result in a systematic underestimate of root
mortality, since roots (especially young ones) are always
more likely to live rather than ¢die. Because of the
tendency for roots to live longer at the Northern site, with
lower overall production, attainment of "equilibirium!
length densities and age distributions would take longer
than at the Southern site. This may be why there seemed to
be little or no "recolonization" effect at the Southern
site, and why our predictions were so accurate. If we
computationally’ adjust (April-October 1989 production and
mortality at the Northern site to reflect the ratio of 1990
mortality and 1990 production to the April 1990 standing
crop (and assuming that equilibrium root length densities
had been attained by April 1990) , we obtain a predicted
October 1989 biomass value of 8440 kg'ha‘l’ a value only 6%

greater than the measured value of 7968.

147

Conclusions

1. Although the major pulses of fine root birth and death
are separated in time in these forests, there is a large
amount of concurrent production and mortality throughout the
growing season. Failure to account for the simultaneity of
these two processes leads to substantial underestimates of
total annual belowground biomass and nutrient production and

turnover.

2. Our data offer further empirical support to the
generally accepted view that the processes of fine root
production and turnover play an important, sometimes
dominant, role in the carbon and N economies of forests.
Roughly 60% of ecosystem NPP is allocated to fine (<2.0 mm
root production) in the two sugar maple forests that we
studied, and fine root turnover is responsible for
approximately 1/2 of carbon and N returned to the soil via

plant litter inputs.

3. Surprisingly, roots <0.5 mm account for a large
proportion of the carbon and nutrients in fine root standing
crops, as well as fine root production and mortality. These
roots play a major role in the carbon and nutrient cycles of
northern hardwood forests, and care should be taken to fully

recover very fine roots in future studies.

148

4. There may to be a consistent relationship between leaf
area and fine root biomass in these forests, probably
reflecting the functional interdependence of the absorbing
and transpiring surface areas of plants. Further
investigations in other forest types and under varying
environmental conditions may reveal differences in patterns
of carbon allocation that are attributable to differential
absorbing/transpiring efficiencies among species, or to
changes in resource allocation elicited in response to

varying environmental factors within a forest type.

5. Given low aboveground productivity during 1989 relative
to other years, and large relative amounts of fine root
production during the same period of time, our observations
support the premise that fine roots and foliage receive
high-priority during resource allocation. Our minirhizotron
and biomass data suggest that fine root dieback probably
occurred during the record 1988 drought, and that fine root
absorbing area was re-established in 1989 at the expense of

bolewood production.

6. Based upon our original predictions for the Southern
site, and our adjusted predictions for the Northern site, it
would appear that root length dynamics measured with
minirhizotrons (once root length densities have stabilized)
closely parallel changes in root biomass, and provide an

index of belowground carbon and nutrient production and

149

turnover. Production and mortality can be directly and
independently measured using minirhizotrons, and changes in
length used to predict the amount of carbon and nutrients

allocated and cycled belowground.

150

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