Oecologia (1997) 111:249±254
Johann G Zaller á John A. Arnone III
Activity of surface-casting earthworms in a calcareous grassland
under elevated atmospheric CO2
Received: 3 November 1996 / Accepted: 11 January 1997
Abstract Earthworms make up the dominant fraction
of the biomass of soil animals in most temperate grass-
lands and have important e€ects on the structure and
function of these ecosystems. We hypothesized that the
e€ects of elevated atmospheric CO2 on soil moisture and
plant biomass production would increase earthworm
activity, expressed as surface cast production. Using a
screen-aided CO2 control facility (open top and open
bottom rings), eight 1.2-m2 grassland plots in Switzer-
land have been maintained since March 1994 at ambient
CO2 concentrations (350 ll CO2 l)1) and eight at ele-
vated CO2 (610 ll CO2 l)1). Cumulative earthworm
surface cast production measured 40 times over 1 year
(April 1995±April 1996) in plots treated with elevated
CO2 (2206 g dry mass m)2 year)1) was 35% greater
(P<0.05) than that measured in plant communities
maintained at ambient CO2 (1633 g dry mass m)2
year)1). At these rates of surface cast production, worms
would require about 100 years to egest the equivalent of
the amount of soil now found in the Ah horizon (top
15 cm) under current ambient CO2 concentrations, and
75 years under elevated CO2. Elevated atmospheric CO2
had no in¯uence on the seasonality of earthworm ac-
tivity. Cumulative surface cast production measured
over the 7-week period immediately following the 6-
week summer dry period in 1995 (no surface casting)
was positively correlated (P<0.05) with the mean soil
water content calculated over this dry and subsequent
wetter period, when viewed across all treatments.
However, no correlations were observed with soil tem-
perature or with annual aboveground plant biomass
productivity. No CO2-related di€erences were observed
in total nitrogen (Ntot) and organic carbon (Corg) con-
centration of surface casts, although concentrations
of both elements varied seasonally. The CO2-induced
J. G. Zaller (&) á J. A. Arnone III
Botanisches Institut, UniversitaÈt Basel,
SchoÈnbeinstrasse 6, CH-4056 Basel, Switzerland
Fax: +41 61 267 35 04; e-mail: zaller@ubaclu.unibas.ch
Ó Springer-Verlag 1997
increase in earthworm surface casting activity corre-
sponded to a 30% increase of the amount of Ntot
(8.9 mg N m)2 vs. 6.9 mg N m)2) and Corg (126 mg C
m)2 vs. 94 mg C m)2) egested by the worms in one year.
Thus, our results demonstrate an important indirect
stimulatory e€ect of elevated atmospheric CO2 on
earthworm activity which may have profound e€ects on
ecosystem function and plant community structure in
the long term.
Key words Carbon dioxide enrichment á Cast
production á Cast C and N á Lumbricidae á
Producer-consumer interactions
Introduction
Ever since the late 1800s, with the pioneering work of
Hensen (1877) and Darwin (1881), earthworms have
been known for the important e€ects they have on the
chemistry and physical structure of soils (e.g. StoÈckli
1928; Edwards and Lofty 1972; Satchell 1983; Lee 1985;
Edwards and Bohlen 1996). Earthworms speed up the
decomposition of plant litter and mineralization of soil
organic matter by reducing the size of detritus particles
for microorganisms (Swift et al. 1979) and by mineral-
izing nutrients directly in their guts (Barley and Jennings
1959; Sharpley and Syers 1977; Syers et al. 1979).
Earthworms can also strongly in¯uence the density, di-
versity and activity of soil microorganisms (e.g. Parle
1963; Scheu 1987; Daniel and Anderson 1992; Brown
1995). Consequently, the productivity of plant commu-
nities has been shown to be enhanced by the presence of
earthworms (Hopp and Slater 1948; Waters 1955;
Stockdill 1982), and data from microcosm studies sug-
gest that earthworms may also signi®cantly in¯uence
plant population dynamics and plant community struc-
ture (e.g. Thompson et al. 1993). Since earthworms
represent the dominant fraction of the biomass of soil
animals in most temperate grasslands (Lee 1985; Curry
1994), they thus have profound e€ects on the structure
250
and function of these ecosystems. In calcareous grass-
lands in Switzerland between 1.5 and 10 t of earthworms
live in each hectare of soil (StoÈckli 1958). More than
70% of these earthworms are surface casting species
which can produce between 20 and 40 t (dry mass) of
nutrient-rich casts per hectare in a single year (e.g.
Glasstetter 1991; ZuÈrcher 1994).
Despite the important role that earthworms play in
many terrestrial ecosystems, we know nothing about
how rising atmospheric CO2 may a€ect their activity and
how altered earthworm activity may feed back on eco-
system processes such as carbon (C) and nitrogen (N)
cycling. Plant CO2 studies which have included animals
such as herbivores have revealed that an understanding
of interactions between plants and animals is essential
for the reliable prediction of the responses of natural
ecosystems to rising atmospheric CO2 (e.g. Fajer et al.
1989; Bazzaz 1990; Johnson and Lincoln 1990; Arnone
et al. 1995). The two most likely e€ects that rising
atmospheric CO2 will have on earthworms are (1)
increases in C supply via stimulated above- and below-
ground plant productivity (cf. Strain and Cure 1985;
Rogers et al. 1994), including litter production (KoÈrner
and Arnone 1992; Owensby et al. 1994; Arnone and
KoÈrner 1995; Navas et al. 1995), and (2) increased soil
water contents (Owensby et al. 1993; Jackson et al. 1994;
P. Niklaus, unpublished work). The latter e€ect appears
to result from decreased stomatal conductance (e.g.
Morison 1987; Jackson et al. 1994; Lauber and KoÈrner
1997) and leaf-level transpiration, leading to decreased
canopy evapotranspiration under elevated CO2 (e.g.
Stocker et al. 1997).
Because earthworms are sensitive to changes in soil
moisture (Evans and Guild 1947; Zicsi 1959; Gerard
1967) and because they feed mainly on plant detritus
(e.g. Waters 1955; Piearce 1978), we hypothesized that
elevated CO2 would stimulate earthworm activity (i.e.
surface cast production), and consequently the amounts
of soil, soil carbon and soil nitrogen egested by earth-
worms. We tested these hypotheses over 1 year in a
calcareous grassland in the second growing season under
elevated CO2 treatment.
Materials and methods
Study site
The calcareous grassland studied here is located on a 20° south-
west-facing slope at an elevation from 500 to 530 m near the village
of Nenzlingen in the Jura Mountains of Switzerland (47°27¢ N,
7°34¢ E). Precipitation from April 1995 to April 1996 was 1060 mm
with a mean annual air temperature of 8.7°C (M. Jaeggi, unpub-
lished work). Up to 1993 this grassland had been used for hundreds
of years as a non-intensively managed pasture, mainly for cattle. It
is no longer grazed but is mown twice a year in early summer and
autumn. Among the approximately 100 vascular plant species
found on this site, the grass Bromus erectus is the dominant species
(Zoller 1954; Leadley and KoÈrner 1996). Soils are classi®ed as a
transition Rendzina (pH is about 6.5, bulk density of the top soil
1.1 g cm)3), with a well developed, stone-free, loamy topsoil and a
rapid transition at 10±15 cm depth to the underlying scree material
(Ogermann et al. 1994). Depth of the Ah-horizon in the experi-
mental plots averages 15 cm.
Experimental design
Eight 1.2-m2 experimental plots have been maintained since March
1994 at current ambient CO2 concentrations (``A'': 350 ll CO2 l)1)
and eight at elevated CO2 (``E'': 610 ll CO2 l)1) using a screen-
aided CO2 control facility (SACC, open top and open bottom
rings; Leadley et al. 1997) as a part of an ongoing, long-term study
at this site (Leadley and KoÈrner 1996). Eight plots have been left
unscreened (``C''). All plots are arranged in a randomized complete
block design with eight blocks. CO2 treatments have been main-
tained round the clock over the whole year except for the period
from 15 December 1995 to 6 March 1996 when air temperatures
were below freezing or when the ground was covered with snow.
SACC screens enabled free movement of most above- and below-
ground fauna into and out of each plot. Further details about the
experimental design can be found in Leadley and KoÈrner (1996).
Precipitation and soil temperature (5 cm depth) were continu-
ously measured near the experimental plots (M. Jaeggi, unpub-
lished work). We also measured soil temperature in each plot
periodically using a portable electronic soil thermometer (5 cm
depth) and correlated these with the continuous measurements to
reconstruct continuous soil temperatures for each experimental
plot. Water content over the top 10 cm of soil in all SACC plots
and four unscreened plots was also continuously monitored using
time-domain re¯ectometry.
Earthworm surface cast production and plant biomass
Surface cast production was measured on average every 9 days
from 5 April 1995 to 12 April 1996 on a permanent 30 cm ´ 30 cm
sampling area in each of the experimental plots. At each sampling,
we recorded in the ®eld the number and fresh mass of newly pro-
duced casts using an electronic pocket balance. After weighing,
each cast was returned to its original position. We then slightly
deformed each cast to facilitate the identi®cation of newly pro-
duced casts at the next sampling date. At least two cast subsamples
from each plot were taken at each sampling date to calculate fresh
mass/dry mass ratios (80°C, 24 h) and for the determination of
organic C (Corg) and total N contents (Ntot, see below). All cast
data are expressed on an oven-dried basis per unit land area (m2).
Vegetation in each plot was harvested down to a height of 5 cm
(typical mowing height) in June and October 1995 and dried at
80°C for 48 h. Plant dry mass is expressed per unit land area.
C and N content of casts
Total C and N content of dried and pulverized cast subsamples was
measured with a CHN analyzer (LECO 1000, St. Joseph, Mich.,
USA). Inorganic C content (Cinorg) of casts was measured using a
hydrochloric acid digestion (cf. Nelson and Sommers 1982) and a
carbonate carbon analyser (LECO CC-1000, St. Joseph, Mich.,
USA). The Corg content of casts was calculated by subtracting the
Cinorg content from the total C measured. According to the cast
production data, we distinguished six earthworm activity periods
over the year and pooled all cast samples from each plot for
chemical analysis.
Statistical analyses
The CO2 treatment e€ect on the rate of surface cast production
(mass and number), cumulative surface cast production, and on C
and N concentrations in casts over time were analyzed using re-
peated measurement ANOVAs (Sokal and Rohlf 1981; SYSTAT
1992). ANOVAs included two CO2 levels (A and E plots) and block
as independent variables. The block factor was deleted from the

model if no statistical signi®cance was indicated (i.e. P > 0.05). We
used unpaired t-tests to identify signi®cant (P O 0.05) CO2 e€ects
on C and N concentrations of casts at individual sampling times. To
assess the relationships between surface cast production and soil
temperature, soil water content (WC) and above-ground plant
biomass productivity, simple linear regression models were ®tted
using data from A and E plots, as well as data from unscreened
plots. We regressed the mean soil temperature calculated over a 13-
week period in 1995, which included 6 weeks without surface casting
and the following 7-week casting period, against the cumulative cast
production over the 7-week casting period. We did the same for soil
WC. We also regressed total annual above-ground plant biomass
production measured over the 1995 growing season against the
cumulative surface cast production from April 1995 to April 1996.
ANOVAs were used to test for the signi®cance of regression co-
ecients of these linear models (Sokal and Rohlf 1981).
Results
Climate and soil conditions
Precipitation and soil temperatures did not di€er be-
tween A and E plots (Fig. 1a) but mean annual soil
water content was 10% greater (P<0.01) in elevated
CO2 plots (33% dry mass) than in ambient CO2 plots
(30% dry mass) (P. Niklaus, personal communication).
Mean soil WC measured in E plots (26.8 ‹ 0.6% dry
mass) over the 6-week-long summer dry period in 1995
was signi®cantly (P<0.05) greater than that measured in
the A plots over the same period (23.3 ‹ 0.8% dry
mass). When averaged over the entire 13-week dry (6
weeks) and subsequent wetter period (7 weeks), soil WC
in E plots was 29.7 ‹ 0.7% and that in A plots was
27.0% ‹ 0.8% (P<0.05).
Fig. 1 a Daily sums of preci-
pitation at the study site (®lled
bars) and mean soil temperatures
in experimental plots (5 cm
depth, averaged across
treatments), b masses and
c numbers of surface casts
produced in a calcareous
grassland exposed to either
ambient (350 ll l)1) or elevated
(610 ll l)1) atmospheric CO2
(means ‹ SE, n = 8).
Earthworm activity periods
denoted by circled numbers
251
Surface cast production and plant biomass
We distinguished six periods of surface casting activity
over the year, each interrupted by a period of inactivity
(Fig. 1b). Rates of cast production (g m)2 day)1 and
number of casts m)2 day)1) ¯uctuated over the year but
with similar patterns observed in plots maintainted at
ambient and elevated CO2 (Fig. 1b, c). Production rates
were highest when soil temperatures at 5 cm depth were
about 17°C and when soils were moist (35% dry mass).
Such periods occurred usually after one to several days
of rains (Fig. 1a, b), and lowest when soils were warm
and dry (above 25°C, water content 24% dry mass).
Rates of surface cast production expressed in g m)2
day)1 in communities maintained at elevated CO2 were
up to 6 times higher than those measured in communi-
ties at ambient CO2 (P<0.05, Fig. 1b). However, dif-
ferences were generally smaller and occurred less
frequently when production was expressed in number of
casts m2 day)1 (Fig. 1c).
Cumulative surface cast production after 1 year (373
days) was 35% greater …P ˆ 0:016† in communities
treated with elevated CO2 (2206 g m)2) than in those
treated with ambient CO2 (1633 g m)2, Fig. 2a). Cu-
mulative cast production measured over the same period
in the unscreened plots was similar to that observed in
elevated CO2 plots (2290 g m)2, data not shown). Cu-
mulative surface cast production measured over the 7-
week period (period 3 in Fig. 2a) immediately following
the 6-week summer dry period (no surface casting) in
1995 was positively correlated (P<0.05) with the mean
soil water content calculated over the entire 13-week
252

Fig. 2 a Cumulative surface

cast production (dry mass) over
1 year b cast Ntot content (mg N
g)1) and c cast Corg (mg C g)1)
content averaged over each of
the six activity periods, denoted
by circled numbers (each bar
represents mean ‹ SE, n = 8
plots) produced in a calcareous
grassland maintained at either
ambient (350 ll l)1) or elevated
(610 ll l)1) atmospheric CO2

Fig. 3 Cumulative surface cast

production (dry mass) over the
6-week period following the
7-week summer inactivity peri-
od (see Fig. 2a) plotted as a
function of: a the mean soil
temperature at 5 cm depth and
b mean soil water content over
the entire 13 weeks. c Total
annual surface cast production
as a function of above-ground
plant biomass production in a
calcareous grassland main-
tained at either ambient (350 ll
l)1) or elevated (610 ll l)1)
atmospheric CO2. P values are
for signi®cance of regressions;
n.s. P>0.05

period, when viewed across all treatments (Fig. 3b,
P ˆ 0:03). However, the same analysis using soil tem-
perature showed no signi®cant correlation (Fig. 3a), nor
was total annual cumulative surface cast production
signi®cantly correlated with annual aboveground plant
biomass production (Fig. 3c).
Aboveground plant biomass production (June plus
October 1995 harvests) was not signi®cantly di€erent in
plots treated with elevated CO2 (367 ‹ 28.3 g m)2) than
in plots maintained at ambient CO2 (306.4 ‹ 23.2 g
m)2; P. Leadley, personal communication).
Cast Ntot and Corg
est in the spring …Ntot ˆ 3:9 mg N gÿ1 ; Corg ˆ 51:4 mg
C gÿ1 †: However, because cumulative cast production
under elevated CO2 summed over the year was 35%
greater than that in plots treated with ambient CO2, so
was the total cumulative land-area-based amount of
Ntot and Corg (28% greater at high CO2 by year's end,
P<0.05). After 1 year, the cumulative amount of N
(Ntot) which was egested by earthworms in surface casts
was 6.9 g N m)2 at ambient CO2 and 8.9 g N m)2 at
elevated CO2 (P<0.05). Over the same period cumu-
lative Corg egested was 93.5 g C m)2 at ambient CO2
and 125.8 g C m)2 at elevated CO2 (P<0.05).

Neither the Ntot nor the Corg concentrations of casts Discussion

were a€ected by CO2 treatment in any of the six
earthworm activity periods (Fig. 2b, c). However, con-
centrations did vary seasonally (P<0.01) with the
highest values measured in the fall and early winter
…Ntot ˆ 5:5 mg N gÿ1 ; Corg ˆ 80 mg C gÿ1 † and the low-
CO2-induced stimulation of soil turnover by earthworms
In 1 year, earthworms produced a mass of surface casts
equivalent to 1.0% of the top 15 cm of surface soil at

ambient CO2 and 1.3% at elevated CO2, assuming a soil
bulk density of 1.1 g cm)3 (e.g. Ogermann et al. 1994).
At these rates of surface cast production, worms in the
ecosystems maintained at current ambient CO2 concen-
trations would require about 100 years to egest the
equivalent amount of soil as that now present in the Ah
horizon (top 15 cm). At elevated CO2 they would need
75 years. Subsurface cast production was apparent on
the outer surface of the minirhizotron tube installed in
each plot, no discernable di€erences between ambient
and elevated CO2 were evident on any of the sampling
dates (J. Arnone, unpublished work). Annual surface
cast production measured in our study (mass basis) av-
eraged across all treatments (about 20 t cast dry mass
ha)1 year)1) was near the bottom of the range reported
for temperate grasslands (e.g. StoÈckli 1928; Evans and
Guild 1947; Bouche 1982; Glasstetter 1991; ZuÈrcher
1994). There are several possible explanations for this.
1. Most data are from managed ecosystems where cast
production is often stimulated by fertilizer application
(Lee 1985; Edwards and Bohlen 1996).
2. Di€erences in climatic conditions when cast produc-
tion is measured can lead to widely di€ering estimates of
cast production at the same site (StoÈckli 1928; Gerard
1967).
3. Finally, earthworm surface cast production is usually
measured by removing the casts produced from the soil
surface. This opens burrow exits and can actually stim-
ulate cast production and lead to overestimation of
production (e.g. Darwin 1881). We removed surface casts
only for weighing in the ®eld but replaced them imme-
diately in their original position. Seasonal oscillations in
surface cast production were not a€ected by CO2 treat-
ments and corresponded to ®ndings from previous
studies conducted in the grasslands of the Jura Moun-
tains (Glasstetter 1991; ZuÈrcher 1994) and in grasslands
in other temperate regions (Evans and Guild 1948; Ger-
ard 1967; NordstroÈm 1975; Nowak 1975; James 1991).
In spite of the long history of earthworm research,
factors which determine earthworm cast production are
not well understood (Lee 1985). Certainly soil moisture
a€ects cast production, but it is unclear whether this is
primarily due to its direct e€ects on earthworm popu-
lations (Bolton and Phillipson 1976; Daniel et al. 1996)
or whether it is indirectly due to moisture-induced
changes in plant biomass and litter production which
a€ects worm food supply (Scheu 1987). In the grasslands
we studied, it appears that soil moisture during dry
periods a€ects worm activity directly (compare Fig. 3b
with Fig. 3c), which would explain the increased earth-
worm activity at high CO2.
CO2-induced stimulation of Ntot and Corg cycling
by earthworms
Despite the lack of di€erences in the concentrations of
Ntot and Corg in surface casts between ambient and
253
elevated CO2, CO2-induced changes of the cumulative
amounts of these elements deposited on the soil surface
in one year by earthworms, in relation to the total
amounts present in the top 15 cm of soil, were sub-
stantial. For example, at elevated CO2 1.6% of the Ntot
pool of the topsoil was egested annually by earthworms
on the soil surface, compared to 1.3% at ambient CO2
(soil bulk density 1.1 g cm)3, soil Ntot ˆ 0:33%,
Ogermann et al. 1994). Similarly, earthworms in eco-
systems maintained at high CO2 egested 2.0% of the
Corg present in the top 15 cm of soil in surface casts
annually, compared to 1.5% at ambient CO2 (soil
Corg ˆ 3:8%, Ogermann et al. 1994). Although we found
no CO2-induced changes of Ntot and Corg concentrations
in surface casts their seasonal increase in the autumn
indicates a functional relationship between earthworm
activity and timing of periods of increased above- and
below-ground plant litter production (Baker and Gar-
wood 1959; Garwood 1967; Kretzschmar 1983). At this
point we do not know whether the amount of available
nutrients in worm casts was signi®cantly a€ected by
elevated CO2.
Thus, the results of our study clearly demonstrate
that elevated atmospheric CO2 can have important in-
direct stimulatory e€ects on the activity of surface
casting earthworms, which in the long term must in¯u-
ence plant community responses to rising atmospheric
CO2. Finally, our results demonstrate the need to in-
clude interactions among organisms when attempting to
predict the e€ects of rising atmospheric CO2 on terres-
trial plant communities and ecosystems.
Acknowledgements We gratefully acknowledge the use of the CO2
enrichment facility provided by the CO2 -team of the University of
Basel (Swiss Priority Program on the Environment). M. Jaeggi
(Geographical Institute, Basel) supplied meteorological data.
P. Jordan helped with statistics. P. Bohlen, S. HaÈttenschwiler,
Ch. KoÈrner, P. Leadley and P. Niklaus provided valuable com-
ments on previous versions of this manuscript. This work was made
possible by grants from the Swiss National Science Foundation
to J.A. Arnone III (NF 3100±042401.94/1) and Ch. KoÈrner
(NF-SPPU 5001-035214).
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