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1341
Ecological Applications,
7(4), 1997, pp. 1341–1349
q
1997 by the Ecological Society of America
EARTHWORM EFFECTS ON CARBON AND NITROGEN DYNAMICS OF
SURFACE LITTER IN CORN AGROECOSYSTEMS
P
ATRICK
J. B
OHLEN
,
1,3
R
OBERT
W. P
ARMELEE
,
1
D
AVID
A. M
C
C
ARTNEY
,
2
AND
C
LIVE
A. E
DWARDS
1
1
Department of Entomology, Ohio State University, Columbus, Ohio 43210 USA
2
Department of Entomology, Ohio Agricultural Research and Development Center, Wooster, Ohio 44619 USA
Abstract.
We examined the influence of earthworms on surface litter decomposition
in corn (
Zea mays
) agroecosystems in Wooster, Ohio. We employed asplit-plot experimental
design with 12 main plots, each 20
3
30 m and containing three 4.5
3
4.5 m field enclosures
in which earthworm populations were (1) increased, (2) decreased, or (3) unmodified. The
main plots received one of three nutrient treatments (cow manure, legume cover crop,
inorganic fertilizer) with four replicates. The three earthworm population treatments were
randomly assigned to the three field enclosures within each main nutrient-treatment plot.
We added corn litter to the soil surface in each of the treatment combinations in the field
enclosures in November 1992 and collected remaining litter after 19, 85, 135, 161, and
191 d. We separated out small piles of surface litter (i.e., ‘‘middens’’) associated with the
entrance to burrows of
Lumbricus terrestris
from the rest of the litter to determine if they
differed from each other in C and N content and microbial activity. We initiated a second
study in the following year (November 1993), adding mechanically shredded corn litter to
the field enclosures and harvesting after 184 d, but without analyzing earthworm middens
separately. Earthworms increased the rate of decomposition of surface litter in both years,
and we estimated that they could have consumed 840 kg·ha
2
1
·yr
2
1
of surface litter. The
C/N ratio of litter remaining on the soil surface (midden plus nonmidden) was significantly
greater in plots with unmodified or increased populations than in enclosures with decreased
populations. However, litter in earthworm middens, which comprised
;
10% of the total
surface litter, had a lower C/N ratio and greater microbial activity than litter in the sur-
rounding area, suggesting that earthworms incorporated litter with the low C/N into their
middens. Because the earthworms feed mainly on litter in their middens, we propose that
they selectively removed litter fractions with a low C/N ratio, thereby increasing the overall
C/N ratio of remaining surface litter. Our results suggest that the redistribution of surface
litter by
Lumbricus terrestris
and its consequences for spatial heterogeneity, microbial
activity, and nutrient content of the litter is a critical process in systems with large pop-
ulations of this earthworm species. These earthworms may exert major control over litter
decomposition in minimally tilled or no-till agroecosystems where they may influence
attempts to manage surface litter.
Key words: carbon and nitrogen dynamics; crop litter; corn agroecosystems; decomposition;
earthworms;
Lumbricus terrestris;
microbial activity.
I
NTRODUCTION
Earthworms are one of the most important groups of
soil fauna in many agroecosystems. Where they are
abundant, earthworms can significantly affect soil
structure, nutrient turnover, and breakdown of organic
matter (Lee 1985, Edwards et al. 1995, Edwards and
Bohlen 1996). Despite the well-known ability of earth-
worms to accelerate litter breakdown, there has been
little research into the effects of different earthworm
species and communities on the breakdown and redis-
tribution of organic matter in agricultural soils. There
is a critical need for research into the effects of earth-
worms on organic matter decomposition in agroeco-
Manuscript received 22 December 1995; revised 2 January
1997; accepted 9 January 1997.
3
Present address: Institute of Ecosystem Studies, Mill-
brook, New York 12545 USA.
systems (Edwards et al. 1995), especially in light of
the trend toward greater adoption of no-tillage practices
and other methods for preserving surface crop litter to
reduce soil erosion (Allmaras et al. 1994).
Lumbricus terrestris
is a common litter-feeding
earthworm species that is capable of removing a sig-
nificant proportion of the total litter inputs in some
ecosystems (Raw 1962, Neilson and Hole 1964). The
incorporation of surface litter into soil by
L. terrestris
can potentially increase the rate of nitrogen mineral-
ization and uptake by plants (Binet and Trehen 1992).
In addition to incorporating plant litter into soil, in-
dividuals of
L. terrestris
also change the spatial ar-
rangement of plant litter on the soil surface by gath-
ering litter into small mounds (known as ‘‘middens’’)
around the entrance to their burrows (Neilson and Hole
1964, Hamilton and Sillman 1989). Earthworm mid-
dens contain a mixture of uningested litter and earth-
1342
PATRICK J. BOHLEN ET AL.
Ecological Applications
Vol. 7, No. 4
worm feces or casts and are a favorable microenviron-
ment for decomposition and a cache of preconditioned
food for the worms. The importance of midden for-
mation in affecting the redistribution of plant litter and
the spatial variability in nutrient dynamics and micro-
bial activity of the litter has not been demonstrated.
Despite the importance of
L. terrestris
in removing and
incorporating surface litter, there is virtually no infor-
mation on how this species influences the nutrient dy-
namics of surface litter, especially in agroecosystems.
The influence of earthworms on nutrient cycling and
organic matter dynamics is difficult to assess, in part
because most studies of earthworm effects on nutrient
cycling processes deal with small-scale phenomena,
such as cycling of nutrients in earthworm casts, where-
as ecosystem processes are defined and measured on a
much larger scale (Lavelle 1988, Anderson 1995, Blair
et al. 1995
b
). It is important to define the scales at
which the regulatory effects of earthworms or other
soil invertebrates on biogeochemical processes emerge
(Anderson 1995), and there is a need for larger scale
experiments in which populations of soil invertebrates
are manipulated and overall ecosystem responses as-
sessed.
In this paper we describe such an experiment in
which we manipulated earthworm populations in large
field enclosures to assess, among other things, the ef-
fect of earthworms on litter decomposition. No studies
have specifically addressed earthworm influences on
nutrient dynamics and redistribution of decomposing
surface litter in agroecosystems, although a few studies
have shown that earthworms in agroecosystems in-
crease the breakdown or mass loss of organic matter
(Syers et al. 1979, MacKay and Kladivko 1985, Par-
melee et al. 1990). Our objectives in this paper are to
examine the extent to which
L. terrestris
regulates de-
composition and nutrient dynamics of surface litter in
agroecosystems, and to relate the observed effects to
what is occurring at the midden microsites created by
individuals of this species. Our decomposition exper-
iments were part of a larger research effort investigat-
ing the influences of earthworms on soil C and N dy-
namics in organically and inorganically fertilized
agroecosystems. Knowledge of those influences and
their interactions with management are critical to the
development of sustainable, biologically based systems
of agricultural production.
M
ATERIALS AND
M
ETHODS
Study site
We conducted our study at the Ohio Agricultural
Research and Development Center in Wooster, Ohio
(41
8
N, 82
8
W). Mean monthly temperatures at this
location range from
2
4.8
8
C in January to 21.2
8
Cin
July, and the mean annual precipitation is 905 mm/yr.
Soil at the site is a fine, mixed, mesic Fragiudalf of the
Canfield series (Luvisol). Canfield soils are deep, gent-
ly sloping, moderately to well-drained silt loam soils
on uplands, with a relatively impermeable fragipan at
a depth of 40–75 cm. The mean percentage organic
matter at the site, determined by wet oxidation, is 3.7
6
0.9%. Soil pH is 6.3
6
0.4 and cation exchange
capacity is 0.1
6
0.02 mol
c
/kg soil. The site was planted
with corn (
Zea mays
) annually between 1984 and 1987
and was used for alfalfa (
Medicago sativa
) production
between 1987 and 1991.
Experimental design
We set up our litter decomposition study in field plots
of a larger experiment investigating the role of earth-
worms in carbon and nitrogen cycling processes in corn
agroecosystems based on organic or inorganic nutrient
inputs. The experiment was a split-plot design in which
different nutrient treatments were the main plot factor
with earthworm population level as the subplot factor.
The main nutrient-treatment plots were 20
3
30 m and
received one of three nutrient treatments, applied just
prior to spring tillage: (1) granular NH
4
NO
3
, (2) straw-
pack cow manure, or (3) legume–rye (
Vicia villosa–
Secale cereale
) cover crop planted in the fall and in-
corporated into the soil by tillage in the spring. We
supplemented the cover crop treatment with alfalfa
(
Medicago sativa
) hay prior to planting the corn crop
in late spring because of poor success in establishing
the cover crop. The three nutrient treatments were rep-
licated four times giving a total of 12 main plots, which
were divided into four blocks of three plots each.
Each of the 12 main nutrient-treatment plots con-
tained three 4.5
3
4.5 m field enclosures in which we
modified earthworm populations. We randomly as-
signed three different earthworm population treatments
among the three enclosures in each plot; earthworm
populations were (1) increased, (2) decreased, or (3)
left unmodified. Walls of field enclosures were poly-
vinyl chloride (PVC) sheets that were buried 45 cm
deep, with 15 cm left above the soil surface. We im-
plemented our field operations (e.g., fertilizer appli-
cation, tillage, crop planting) with typical farm ma-
chinery in the main nutrient-treatment plots and by
hand in the earthworm enclosures.
We manipulated earthworm populations in the spring
and fall of 1991, 1992, and 1993, using an electro-
shocking technique to decrease earthworm populations
and additions of field-collected earthworms to enclo-
sures to increase populations (Bohlen et al. 1995). The
other earthworm treatment was a control, in which we
did not modify earthworm populations. Preliminary
tests and regular sampling for other soil invertebrate
groups (nematodes, enchytraeids, microarthropods)
showed that those groups were not affected by elec-
troshocking (Blair et al. 1995
a
). Twice per year, we
sampled earthworm populations in enclosures using a
combination of hand sorting and formalin extraction
(Blair et al. 1996). Worms were preserved in 5% for-
malin, identified, counted, and oven-dried at 60
8
C.
November 1997 1343
EARTHWORMS AND LITTER DECOMPOSITION
Litter decomposition experiments
We conducted two separate litter decomposition ex-
periments, one started in 1992 and the other in 1993.
The purpose of the second experiment was to verify
results from the first year and examine annual vari-
ability in decomposition at the site. In the first exper-
iment, we sampled litter over several dates to establish
temporal dynamics. Additionally, in the first experi-
ment, we examined earthworm middens in detail to
determine their influence on the spatial distribution of
litter quality and decomposition. In the second exper-
iment, we sampled litter only once and did not separate
earthworm middens from the total surface litter pool.
Litter decomposition, 1992–1993.
—The first decom-
position experiment was started in autumn 1992 and
ended when the plots were tilled in spring 1993. Corn
litter, consisting of an equal mixture of stalks and
leaves, was obtained from whole plants harvested man-
ually on 15 October 1992 and oven-dried at 60
8
C; the
corn plants were cut manually into 5–10 cm long pieces
and then sieved (10 mm mesh) to remove smaller frag-
ments. On 10 and 11 November 1992, in each of the
36 enclosures, we cleared 12 areas of existing surface
litter, each 0.1 m
2
, and covered them with a mixture of
35 g each of the oven-dried corn stalks and leaves, for
a total of 70 g. We enclosed the litter with rings of
flexible aluminum strips, which we pressed 1–2 cm into
the soil and covered with plastic mesh (1 cm). The total
amount of litter added to the rings was based on the
amount of corn litter left in the field after harvest (
;
700
g oven-dry mass/m
2
).
We collected the litter after 19, 85, 135, 161, and
191 d in the field (i.e., 30 November, 7 February, 26
March, 21 April, and 21 May) from two litter rings per
enclosure on the first three sample dates and from three
rings per enclosure on the final two dates. For each
litter ring that contained earthworm middens, we care-
fully collected surface litter not associated with the
middens into one sample bag, then counted the middens
and combined the litter from the middens into a sep-
arate bag. The collected litter was dried at 60
8
C,
weighed and ground through a 200
m
m-mesh screen.
Litter associated with earthworm middens was thor-
oughly mixed with soil, and required further treatment
before drying and weighing. We placed the samples in
a 2-L glass beaker and treated them with just enough
volume of a 0.5% metaphosphate solution to cover the
litter and disperse adhering soil particles. We stirred
the litter briefly (
,
15 s) to minimize leaching, poured
it over a 1-mm mesh sieve, and rinsed it briefly with
deionized water. The washed samples were dried at
60
8
C, weighed and then ground through a 200-
m
m
screen.
The carbon and nitrogen content of all litter samples
was determined on a NA 1500 Series 2 Automatic Ni-
trogen, Carbon Analyzer (Carlo Erba Instruments, Mi-
lan, Italy). We corrected for soil contamination of the
litter samples using the ash-free dry mass of litter and
soil as described by Blair and Crossley (1988).
Litter decomposition, 1993–1994.
—In the second
decomposition experiment we harvested corn plants
manually and passed them through a gasoline-powered
shredder, producing litter material with fragments that
were smaller and more shredded than the material used
in the first year. We oven-dried (60
8
C) the litter and
sieved (6 mm) it to remove small fragments. On 10
and 11 November 1993, we placed 70 g of the shredded
oven-dried corn litter over cleared 0.1-m
2
quadrats in
the earthworm enclosures, holding the litter in place
with plastic mesh secured by metal stakes. We collected
the litter from the quadrats after 184 d (4 May 1994),
and processed it as described previously, except that
we did not collect or analyze earthworm middens sep-
arately.
Substrate-induced respiration on corn litter
During the first decomposition study (1992–1993),
we used a substrate-induced respiration (SIR) tech-
nique (Beare et al. 1990) to compare the microbial
activity of litter that was associated with earthworm
middens to litter that was not. We performed SIRassays
on subsamples of freshly collected litter, which were
stored at 4
8
C for
;
48 h prior to the assays. We made
11 paired comparisons between litter in earthworm
middens and litter not in middens for litter collected
on days 135, 161, and 191. We excluded corn stalks
from these comparisons, because earthworms gathered
mainly leaves, not stalks, into their middens. We care-
fully removed soil particles from the litter by hand prior
to the SIR assays, and then put an equivalent of 1 g
oven-dry mass of litter into 125-mL Erlenmeyer flasks.
We then added 5 mL of glucose solution (80 mg/g dry
litter) uniformly over the litter with a syringe, stop-
pered the flasks immediately and allowed them to equil-
ibrate for 30 min. We then connected the flasks to a
continuous flow-through respirometer adapted from
Cheng and Coleman (1989) and incubated the litter
samples for 2.5 h at 22.0
6
0.5
8
C. The air entering the
flasks contained no CO
2
, and the CO
2
respired during
the incubation was trapped in 50 mL of alkali solution
(0.04 N-NaOH). We titrated the alkali traps with 0.04
N-HCl to determine the total CO
2
produced during the
incubation.
Statistical analysis
We used a General Linear Model (SAS Institute
1985) for a split-plot design to test effects of the earth-
worm population treatments, nutrient treatments, and
interactions between nutrient and earthworm treat-
ments on the nutrient dynamics of decomposing surface
litter, using data from all dates independently. The in-
teraction between nutrient treatment and block was
used as the error term for determining the significance
of nutrient treatment effects. The analyses used the
mean values averaged from the quadrats in each field
1344
PATRICK J. BOHLEN ET AL.
Ecological Applications
Vol. 7, No. 4
F
IG
. 1. (A) The mean number and (B) the mean dry mass
of earthworms per square meter in the autumn of 1993 in
field enclosures with decreased, unmodified, or increased
earthworm populations (data are from Bohlen et al. 1995).
The error bars show 1
SE
.
enclosure. We transformed all ratios and percentages
with an arcsine-square-root transformation prior to
analysis. We used Tukey’s hsd mean separation tests
to determine differences among means, and a Student’s
paired
t
test to compare the SIR rates of the litter in
earthworm middens to those of litter not in middens.
R
ESULTS
Earthworm populations
Field enclosures with decreased earthworm popu-
lations had
;
28% as many earthworms and 30% as
much earthworm biomass compared to populations in
enclosures with unmodified populations (Fig. 1). Earth-
worm biomass was
;
1.5-fold greater in enclosures
with increased populations than in those with unmod-
ified populations, due mainly to an increase in the bio-
mass of
L. terrestris.
Of the four species present (
Apor-
rectodea trapezoides, Aporrectodea tuberculata, Lum-
bricus terrestris,
and
Lumbricus rubellus
),
L. terrestris
was the only surface-litter-feeding species that com-
prised a significant proportion of total earthworm bio-
mass (Fig. 1). The other major species at the site,
A.
tuberculata,
is a geophagous species that feeds mainly
on organic matter incorporated in the soil, not surface
litter (Edwards and Bohlen 1996). More detailed in-
formation on the earthworm populations can be found
in Bohlen et al. (1995).
Nutrient treatments
The nutrient treatments had no significant effect on
the mass loss or nutrient dynamics of corn litter, nor
was there a significant interaction between the nutrient
treatments and earthworm population treatments. After
three consecutive annual applications of the nutrient
treatments, there were no significant differences be-
tween nutrient treatments in earthworm population den-
sity or biomass (Bohlen et al. 1995). For these reasons,
we will not discuss the nutrient treatments any further.
Litter decomposition
Corn litter added to the litter rings in 1992 had an
average C/N ratio of 57.7. The corn leaves contained
over twice as much N (1.09%) as did corn stalks
(0.45%). Litter used in 1993 had a lower initial N con-
tent (0.63) and a correspondingly greater C/N ratio
(70.69) than did the litter used in 1992. The litter lost
;
40% of its initial C and
;
70% of its initial N during
191 d in the field in 1992–1993 (Fig. 2), and lost 40–
50% of its initial carbon and 50–60% of its initial N
during 184 d in 1993–1994 (Table 1).
We estimate that earthworms removed a total of 420
kg/ha of surface corn litter from November 1992 to
May 1993. During both decomposition experiments,
earthworms increased the rate of loss of both C and N
from surface litter (Table 1, Fig. 2). Their effect on the
loss of litter N was greater than their effect on the loss
of litter C, so that the C/N ratio of the total surface
litter pool was significantly greater in enclosures with
increased or unmodified populations than in those with
decreased populations, in both years (Table 1, Fig. 2).
Differences between plots with decreased populations
and those with either increased or unmodified popu-
lations were greater in the second year (1993–1994)
than in the first year for both C and N remaining in
surface litter (cf. Table 1 and Fig. 2).
Earthworm middens.
—Plots with increased earth-
worm populations had the most earthworm middens
throughout the 1992–1993 study period and plots with
decreased earthworm populations had the fewest earth-
worm middens (Fig. 3). In general, the number of mid-
dens in plots with increased and unmodified popula-
tions were not significantly different. Averaged over
all five sample dates, the mean numbers of middens
were 20.5, 48.8, and 67.5 m
2
in plots with decreased,
unmodified, and increased populations, respectively.
The total amount of corn litter in earthworm middens
(Fig. 4) and the percentage of the total remaining litter
C and N that was associated with earthworm middens
(Table 2) were significantly lower in plots with de-
creased earthworm populations than in plots with in-
creased or unmodified populations. The C/N ratio of
corn litter in earthworm middens was significantly low-
November 1997 1345
EARTHWORMS AND LITTER DECOMPOSITION
F
IG
. 2. (A) The mean percentage of initial carbon and
nitrogen in corn litter remaining, and (B) the C/N ratio of the
litter through time in field enclosures with decreased, un-
modified, or increased earthworm populations (mean
6
1
SE
,
n
5
12). Asterisks indicate significant differences among
earthworm treatments for a given sample date (
P
,
0.05,
Tukey’s hsd test). The data are for the study started on 10
November 1992.
T
ABLE
1. Effects of the earthworm population manipula-
tions on the carbon and nitrogen remaining and the C/N
ratio (
X
¯
6
1
SE
,
n
5
12) of corn litter after 184 d in 1993–
1994. Data for 1992–1993 are shown in Fig. 2.
Earthworm
population
treatment Initial C
remaining (%) Initial N
remaining (%) Litter
C/N
Decreased
Unmodified
Increased
58.54
a
6
1.61
52.87
b
6
1.58
51.30
b
6
1.97
51.54
a
6
3.21
39.82
b
6
2.89
38.80
b
6
1.25
82.93
b
6
4.32
97.35
a
6
4.87
93.57
a
6
2.56
Note:
Values in the same column followed by a different
superscript letter are significantly different (
P
,
0.05).
T
ABLE
2. The mean percentage of the total carbon and nitrogen of remaining litter that was
associated with earthworm middens, 19 and 191 d after litter was placed in the field (1992–
1993 experiment), in plots with the three different earthworm treatments (
X
¯
6
1
SE
,
n
5
12).
Earthworm
population
treatment
C in midden litter
(% of total litter C)
19 d 191 d
N in midden litter
(% of total litter N)
19 d 191 d
Decreased
Unmodified
Increased
2.56
b
6
0.68
6.17
a
6
0.64
5.72
a
6
0.68
2.62
b
6
0.35
8.42
a
6
1.20
6.96
a
6
0.76
5.08
b
6
1.23
12.59
a
6
1.14
10.80
a
6
1.07
4.89
b
6
0.53
12.51
a
6
1.50
10.58
a
6
0.95
Note:
Values in a column followed by a different superscript letter are significantly different
(
P
,
0.05).
er than that of litter not associated with middens at all
earthworm population levels (Table 3). In plots with
decreased earthworm populations the C/N ratio of all
litter, whether in middens or not in middens, was lower
than in plots with unmodified or increased earthworm
populations (Table 3).
Middens also had an influence on microbial activity.
The litter in earthworm middens had SIR rates that were
2.16, 1.85, and 1.41 times greater than those of litter
that was not in the middens, on days 135, 161, and
191, respectively (Fig. 5). The SIR rates of the litter
increased progressively from day 135 to 191 (i.e., from
March to May 1993).
D
ISCUSSION
Influence of earthworms on litter carbon and nitro-
gen dynamics.
—Our results demonstrated that earth-
worms not only increased the rate of loss of surface
litter, but also significantly altered the C/N ratio of the
litter remaining on the soil surface. Plots with de-
creased earthworm populations had the greatest amount
of litter remaining on the soil surface, and litter in those
plots had the lowest C/N ratio among the three earth-
worm population treatments in both years.
The lower C/N ratio of litter in earthworm middens
relative to surrounding litter in our experiment could
have been due to earthworms selecting litter with a
lower C/N ratio, to the C/N ratio of the litter decreasing
after incorporation into middens, or to a combination
of those two processes. However, the litter in middens
had a much lower C/N ratio (43:1) than did the sur-
rounding litter (91:1) only 19 d after the litter was
placed in the field and before any significant chemical
or microbial changes in the litter could have taken
place, suggesting that the earthworms selected litter
with a lower C/N ratio. Because worms feed from their
middens (Darwin 1881), they would have selectively
removed material with a low C/N ratio from the total
surface litter pool (i.e., midden litter plus surrounding
1346
PATRICK J. BOHLEN ET AL.
Ecological Applications
Vol. 7, No. 4
F
IG
. 3. The mean number of earthworm
middens per square meter (mean
1
1
SE
,
n
5
12) in plots with decreased, unmodified, or in-
creased earthworm populations. Different let-
ters above bars indicate significant differences
among treatments for a given sample date (
P
,
0.05, Tukey’s hsd test). The data are for the
study started on 10 November 1992.
F
IG
. 4. The mean amount of litter (mean
1
1
SE
,
n
5
12) in earthworm middens on five
consecutive sample dates in the 1992 study in
plots with decreased, unmodified, or increased
earthworm populations. For each sampling date,
bars labeled with different letters are signifi-
cantly different (
P
,
0.05, Tukey’s hsd test).
litter), thus increasing the overall C/N ratio of the re-
maining surface litter. This explanation resolves the
apparent contradiction between the effects of earth-
worms decreasing the C/N ratio of litter in their mid-
dens but increasing the C/N ratio of the total surface
litter pool. Alternatively, the elevated microbial activ-
ity of litter in middens relative to surrounding litter
after several months in the field indicates that litter in
middens was modified after becoming incorporated
into middens. Thus, both processes, litter selection and
modification of the litter, may have contributed to the
lower C/N ratio of litter in the middens, the net effect
being the creation of high-quality (i.e., low C/N ratio)
patches of litter from which the earthworms fed. Fur-
ther tests that explicitly assess litter selection and feed-
ing by the earthworms are needed to provide more con-
clusive evidence for litter selection than we have dem-
onstrated in the current study.
Earthworms have been shown to have a preference
for litter with a low C/N ratio in some feeding trials
(Satchell and Lowe 1967, Hendricksen 1990, Edwards
and Bohlen 1996). Although we did not directly mea-
sure litter selection by earthworms in our experiment,
we showed that litter in earthworm middens, which is
where the worms do most of their feeding, had much
lower C/N ratios than did the surrounding litter. Similar
results have been reported for middens in deciduous
forests (Szlavecz 1985).
Other studies have shown that earthworms accelerate
the breakdown of organic matter in agroecosystems,
but none have examined changes in the C/N ratio of
surface litter due to earthworm activity and the spatially
dynamic processes coupled to midden formation.
Lum-
bricus rubellus
increased the rates of disappearance of
soybean and corn litter over treatments without earth-
worms by 165 and 320%, respectively, in a 36-d pot
experiment (MacKay and Kladivko 1985). Earthworm
populations in a no-till agroecosystem in Georgia,
November 1997 1347
EARTHWORMS AND LITTER DECOMPOSITION
T
ABLE
3. Carbon-to-nitrogen ratios (
X
¯
6
1
SE
,
n
5
12) of
the corn litter associated with earthworm middens, and lit-
ter not associated with middens, 191 d after the litter was
placed in the field (1992–1993 experiment).
Earthworm
population
treatment
Carbon-to-nitrogen ratio†
Litter in middens Litter not in middens
Decreased
Unmodified
Increased
53.10
b
6
1.98
74.53
a
6
2.92
77.10
a
6
2.44
105.45
b
*
6
2.86
122.31
a
*
6
3.23
124.72
a
*
6
4.23
Note:
Values in the same column followed by a different
letter are significantly different (
P
,
0.05, Tukey’s hsd test).
Asterisks indicate significant differences between values
within a row (
P
,
0.05, paired
t
test).
† The C/N ratio for total litter (midden plus nonmidden)
is shown in Fig. 2.
F
IG
. 5. The mean amount of CO
2
respired (micrograms
per gram of litter per hour) during a substrate-induced-res-
piration (SIR) assay with corn litter that was either associated
or not associated with earthworm middens in the spring of
1993. Respiration rates were significantly higher in the litter
associated with earthworm middens on each sample date (
P
,
0.05, paired
t
test).
United States, significantly decreased amounts of fine,
coarse, and total particulate organic matter in the soil
(Parmelee et al. 1990). A mixed community of
L. ru-
bellus
and
Aporrectodea caliginosa
removed at least
80 kg·ha
2
1
·d
2
1
of surface litter in a New Zealand pas-
ture during the period of their highest seasonal activity,
and removed an annual total of 6100 kg·ha
2
1
·yr
2
1
(Syers et al. 1979). We estimated from our data that
earthworms removed a total of 420 kg/ha of corn litter
from November 1992 to May 1993. Since earthworms
were active for only 4 mo of that time period, and are
generally active for 8 mo/yr, they have the potential to
consume at least 840 kg·ha
2
1
·yr
2
1
of corn litter at our
site. Furthermore, our results show that earthworms not
only enhance litter breakdown but also alter the nutrient
ratios of the litter that remains, possibly due to selective
feeding activities.
Microbial activity in earthworm middens.
—The
greater substrate-induced respiration (SIR) rates in the
midden litter as compared to litter not in middens sug-
gests that microbial biomass and decomposition rates
were greater in the middens, because SIR rates are a
good predictor of total microbial biomass and decom-
position rates (Beare et al. 1990, 1991). The SIR rates
in our study were negatively and linearly related to
C/N ratio of the litter, with correlation coefficients of
2
0.87,
2
0.57, and
2
0.77 (
P
,
0.05, in all cases) for
the three consecutive sample dates on which they were
measured. However, the SIR rates were not signifi-
cantly correlated with the C/N ratio of litter when data
from all three sample dates were analyzed together,
which suggests that there was not a simple relationship
between litter microbial activity and C/N ratio.
Litter in the middens was mixed with earthworm
casts, which have increased amounts of available nu-
trients and microbial biomass relative to surrounding
soil, and may therefore act as an microbial inoculum
of the litter (Parle 1963, Scheu 1987, Tiwari et al. 1989,
Lavelle and Martin 1992). Earthworm middens contain
earthworm excretory products and mucus, which pro-
vide nutrient and energy sources for microbial popu-
lations. Earthworms also shred materials in their mid-
dens (Darwin 1881), exposing a greater surface area
to microbial attack. Taken together, the biotic inter-
actions in the middens suggest that midden formation
is a special instance of ‘‘feedback’’ regulation of re-
source quality (sensu Swift et al. 1979) in which earth-
worms modify the litter resource in a way that enhances
microbial activity and decomposition, ultimately im-
proving the quality of the litter as a food source for
the worms.
Contribution of earthworms to litter nitrogen loss.
—
Our results indicate that earthworms, in particular
L.
terrestris,
can make a significant contribution to nitro-
gen loss from surface litter, even during the relatively
inactive period from late fall to early spring. The total
contribution of earthworms to nitrogen removal from
surface litter was estimated by comparing the amount
of litter nitrogen remaining in control enclosures with
that remaining in the few enclosures where electro-
shocking had effectively eliminated earthworm popu-
lations. There was a total of 44.1 kg N/ha in surface
litter at the beginning of the 1993–1994 decomposition
experiment. After 184 d, 25.5 kg N/ha remained in
surface litter in enclosures with no earthworms, where-
as 17.6 kg N/ha remained in surface litter in enclosures
with unmodified earthworm populations. Thus, be-
tween November and May, earthworms increased N
removal by an estimated 1.4-fold. We arrived at similar
estimates for data from the 1992–1993 experiment.
What was the fate of the nitrogen removed by earth-
worms from the surface litter? We did not trace the
ultimate fate of the nitrogen in surface litter, butresults
of S. Subler et al. (
unpublished manuscript
) suggest
that some of the nitrogen ‘‘lost’’ from surface litter
may have ended up as microbial biomass and mineral
1348
PATRICK J. BOHLEN ET AL.
Ecological Applications
Vol. 7, No. 4
nitrogen forms in the soil beneath earthworm middens.
They showed that a large portion of the extractable
nitrogen, dissolved organic nitrogen, total carbon and
nitrogen, and microbial activity in the top 5 cm of soil
were within a few centimeters of earthworm middens.
Thus, the spatial pattern in surface litter created by
earthworm middens is linked directly to spatial patterns
in soil nutrient pools and microbial activity. Experi-
ments with isotopically labeled plant litter are needed
to determine whether plant litter in earthworm middens
contributes to the elevated concentrations of nitrogen
beneath the middens.
Implications for litter management in agroecosys-
tems.
—The influence of earthworms on the decom-
position of surface litter in agroecosystems is important
in light of recent interest in managing crop litter to
reduce soil erosion and otherwise improve soil quality
(Allmaras et al. 1994). Even more pronounced effects
of earthworms on surface litter dynamics than were
observed in the current study are likely to occur in
no-tillage agroecosystems, which are being adopted
more widely (Sprague and Triplett 1986) and which,
in addition to increasing the amounts of crop litter on
the soil surface, also enhance earthworm populations
(Gerard and Hay 1979, Barnes and Ellis 1982, Edwards
and Lofty 1982, House and Parmelee 1985). Earth-
worms can work against the goal of maintaining an
even, protective cover of litter on the soil surface in
row-crop agroecosystems, with potential consequences
for soil erosion. This was observed in a forest ecosys-
tem where an increase in sediment loss was associated
with bare patches of soil created between middens of
L. terrestris
(Hazelhoff et al. 1981), and similar effects
may occur in some agroecosystems.
Earthworms often are not included in studies or mod-
els of crop litter decomposition (e.g., Smith and Peck-
enpaugh 1986, Broder and Wagner 1988, Douglas and
Rickman 1992), despite their potential to have large
effects on decomposition in many agroecosystems. Our
results indicate that earthworms can significantly in-
crease surface litter decomposition even during winter
and early spring, when faunal effects on decomposition
are thought to be relatively less important than micro-
bial effects (Stott et al. 1990). Evidence from our study
and the work of others (MacKay and Kladivko 1985,
Zachmann and Linden 1989, Parmelee et al. 1990) sug-
gests that earthworm influences need to be considered
when investigating the decomposition and nutrient dy-
namics of surface litter in agroecosystems with large
populations of litter-feeding earthworms.
A
CKNOWLEDGMENTS
We express our gratitude to M. Allen and J. Long for as-
sistance with field and laboratory work. We thank P. Groff-
man, S. Subler, B. Stinner, J. Blair, R.Boerner, andtwo anon-
ymous reviewers for providing critical comments that helped
improve this paper. This project was part of the doctoral work
of P. Bohlen and was supported by a grant from The National
Science Foundation (DEB 9020461).
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