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Ecology, 80(3), 1999, pp.

873–881
q 1999 by the Ecological Society of America

INTERACTIONS BETWEEN PLANT SPECIES AND EARTHWORM CASTS IN


A CALCAREOUS GRASSLAND UNDER ELEVATED CO2
JOHANN G. ZALLER1 AND JOHN A. ARNONE III2
Botanisches Institut, Universität Basel, Schönbeinstrasse 6, CH-4056 Basel, Switzerland

Abstract. We tested the hypothesis that the spatial proximity of a plant species to
nutrient-rich earthworm casts (e.g., 100% more ammonium and 30% more phosphate than
in adjacent soil) is an important determinant of a plant’s responsiveness to elevated at-
mospheric CO2. In 1995 we mapped the location of both earthworm surface casts and plants
in each of 16 1.2-m2 plots in a species-rich calcareous grassland in northwestern Switzerland.
Eight plots have been maintained under current ambient CO 2 concentrations (350 mL CO2/
L), and eight have been maintained at elevated CO2 (600 mL CO2/L) since March 1994. In
addition, total ramet production of each species, as a measure of performance, and cu-
mulative cast production at each location (cell) were recorded at peak community biomass
in 1995. Plant species within functional groups (graminoids, non-legume forbs, and leg-
umes) differed markedly in their degree of association with casts; however, after two
growing seasons elevated CO2 had no effect on plant species or functional group associations
with casts. No statistically significant relationship could be demonstrated between plant-
species response (i.e., ramet production) to elevated CO 2 and the degree of association with
casts within any of the functional groups. However, a positive relationship was observed
between the mean response of graminoid species to elevated CO 2 (measured as the per-
centage change in mean total ramet production of graminoid species, relative to mean total
ramet production at ambient CO2) and their mean degree of association (%) with surface
casts at ambient CO2. Thus, graminoid species more frequently associated with casts (e.g.,
Anthoxanthum odoratum and Carex caryophyllea) produced more ramets per square meter
at elevated CO2 than those less frequently associated with casts (e.g., Agrostis tenuis and
Danthonia decumbens). These results, along with the strong and significant positive cor-
relations observed between ramet production and associated cumulative cast mass across
CO2 treatments for most plant species in all functional groups demonstrate: (1) that plant
species differ significantly in their degree of association with nutrient-rich earthworm sur-
face casts, regardless of the relative abundance of plant species in the community; (2) that
graminoid species that are more highly associated with casts may respond more strongly
to rising CO2 than those less highly associated with casts; and (3) that nutrient-rich earth-
worm casts stimulate the growth (ramet production) of most plant species in these grassland
communities, even at current levels of atmospheric CO2. The data further suggest that these
species-specific relationships between plants and casts have helped define the current struc-
ture of these highly diverse grassland communities and will likely influence their future
structure as global CO2 levels continue to rise.
Key words: CO2 enrichment; earthworm activity; earthworm surface casts; elevated CO2, plant
species responses; fertile soil microsites, role of earthworm casts; global warming, plant species
responses; Lumbricidae; plant–animal interactions; plant–cast spatial distribution; soil ecology; spa-
tial distribution of plants, earthworm effects.

INTRODUCTION Körner and Bazzaz 1996). These interactions are in-


fluenced strongly by soil fertility, with species in low-
Numerous studies suggest that rising atmospheric
fertility ecosystems responding more slowly than those
CO2 will alter the competitive interactions among plant
in high-fertility systems (Körner 1996, Reynolds
species and thus lead to changes in the structure and
1996). However, low nutrient supply may not neces-
composition of plant communities (e.g., Bazzaz 1990, sarily preclude pronounced effects on plant community
structure in the long term (Leadley et al. 1998). In the
Manuscript received 10 November 1997; revised 6 April grassland communities we studied, causes for changing
1998; accepted 13 April 1998; final version received 18 May species abundance are numerous but may ultimately
1998. derive from species-specific gas-exchange responses to
1 Present address: Department of Rangeland Resources and
elevated CO2 (Lauber and Körner 1997). However, in-
The Ecology Center, Utah State University, Logan, Utah
84322-5230 USA. E-mail: jgz@cc.usu.edu direct effects of elevated CO2, such as increases in soil
2 Present address: Biological Sciences Center, Desert Re- moisture (Niklaus et al. 1998) and greater inputs of
search Institute, P.O. Box 60220, Reno, Nevada 89506 USA. carbon to the rhizosphere (e.g., Hungate et al. 1997,
873
874 JOHANN G. ZALLER AND JOHN A. ARNONE III Ecology, Vol. 80, No. 3

Meier et al. 1997) may be more important determinants Switzerland (520 m; 478279 N, 78349 E) on a southwest-
of competitive outcome because of their secondary ef- facing slope (208). Annual precipitation averages 900
fects on soil heterotrophs. mm, with mean annual air temperatures between 8.58
Indeed, increased soil water content under elevated and 9.08C (Ogermann et al. 1994). The grassland is
CO2 appears to be the major cause of the 35% increase dominated by the tussock grass Bromus erectus but
in earthworm activity (5.7 3 103 kg more surface-cast contains .75 other vascular plant species (Huovinen-
dry mass produced per hectare measured over one year) Hufschmid and Körner 1998). Until 1993 the area was
we observed in calcareous grasslands (Zaller and Ar- managed mainly as cattle pasture. Since then it has been
none 1997). This increased activity corresponded to a mown annually in early summer and early fall. Mean
30% increase in total N and C egested by earthworms aboveground net primary productivity is ;400 g·m22·yr21,
at our site, 70% of which are known surface-casting 70% of which is represented by graminoid species
species (Zürcher 1994; J. Zaller, unpublished data). (Huovinen-Hufschmid and Körner 1998, Leadley et al.
These casts often contain higher concentrations of 1998). Soils are classified as a transition Rendzina with
plant-available nutrients (e.g., Puh 1941, Aldag and a well-developed, stone-free, loamy topsoil (Ah hori-
Graff 1975) than does the surrounding soil, and may zon: pH 6.5, bulk density of 1.1 g/cm3, organic carbon
represent nutrient-rich microsites that plants can ex- content 3.2%, C:N ratio ;12) and a rapid transition
ploit. Casts may even contain plant growth substances
near 15 cm depth to the underlying scree material
(Gavrilov 1963, Nielson 1965, Tomati et al. 1988). In
(Ogermann et al. 1994).
many plant communities, nutrient-rich soil microsites
Since March 1994 eight plant communities on 1.2-
represent a valuable source of mineral nutrients (Chap-
m2 hexagonal experimental plots have been maintained
in 1980, Grime et al. 1986, Caldwell et al. 1991). A
at current ambient CO2 concentrations (‘‘A,’’ 350 mL
plant’s ability to exploit such spatially and temporally
heterogeneous soil resources, either through enhanced CO2/L) and eight at elevated CO2 (‘‘E,’’ 600 mL CO2/
fine-root proliferation (e.g., Drew and Saker 1975, St. L) using the Screen Aided CO2 Control technology
John et al. 1983, Crick and Grime 1987, Jackson and (SACC, Leadley et al. 1997). Each SACC unit con-
Caldwell 1989, Jackson and Caldwell 1992, Bilbrough sisted of a 50-cm-tall 3 1.2-m-diameter (hexagonal)
and Caldwell 1997) or improved uptake kinetics (Jack- transparent plastic screen (open bottom and open top),
son et al. 1990, Jackson and Caldwell 1991) can affect and a pipe at the base of the screen through which CO2-
the competitive balance among species in a community enriched air is directed into the unit. Plots were ar-
(e.g., Jackson and Caldwell 1992, Bilbrough and Cald- ranged over an area of 1400 m2 in a randomized com-
well 1997). Actually, fine roots have been observed to plete block design with eight blocks (i.e., one A and
proliferate extensively in earthworm casts (Springett one E plot per block). CO2 treatments were maintained
and Syers 1979, Spiers et al. 1986, J. Zaller, personal continuously, except during the winter months (De-
observation), and at our grassland site the distribution cember to March) when CO2 enrichment was stopped.
of surface casts and plant species are spatially quite
heterogeneous at scales of less than 1 m. These patterns Plant species spatial distribution and ramet
led us to test several hypotheses related to the spatial production
relationships between plants and casts that may deter- We determined the presence or absence of vascular
mine species’ responses to elevated CO2. plant species in each of 100 3 3 3 cm cells in a 30 3
We tested the hypothesis that plant species more 30 cm area in each experimental plot from 19 July to
highly associated with surface casts would respond 1 August 1995 (Fig. 1, top). The frequency of each
more positively to elevated CO2 by producing more species was expressed as the percentage of the cells in
ramets, than species less associated with casts, because which any part of a plant of that species was rooted
of greater nutrient availability in casts relative to ad- (i.e., rooted frequency, Greig-Smith 1983). The number
jacent soil. The objectives of our study were to deter- of ramets of each plant species in each cell also was
mine: (1) whether plant species or functional groups counted as an indicator of performance and growth
in these grassland communities differ in their associ- potential of that species. The response of each plant
ation with surface casts at current ambient atmospheric species to elevated CO2 was calculated for each block
CO2 concentrations, (2) whether elevated CO2 alters as the difference between the total number of ramets
these associations, (3) if species and functional groups observed in the 30 3 30 cm area at ambient CO2 and
more closely associated with casts produce more ramets the total number observed at elevated CO2 divided by
under elevated CO2 than those less closely associated,
the total number observed at ambient CO2, expressed
and (4) how well production of ramets among plant
as a percentage. Each plant species was assigned to one
species and functional groups is related to the asso-
of three functional groups based on taxonomy—gra-
ciated cast mass.
minoids (Poaceae, Cyperaceae and Juncaceae), non-
MATERIALS AND METHODS leguminous forbs, and leguminous forbs—to assess
Study site, CO2 enrichment, and experimental design whether relationships with casts and responses to el-
We conducted this study in a species-rich calcareous evated CO2 occurred at this more aggregated level of
grassland in the Jura Mountains located near Basel, plant community organization. Only plots in which a
April 1999 PLANT–EARTHWORM INTERACTIONS AT HIGH CO2 875

FIG. 1. Schematic diagram of method used


to collect plant and cast data (grid cell size: 3
3 3 cm). Ramets of each plant species were
counted if its roots were present in a grid cell.
Cumulative earthworm surface cast production
was calculated for each cell over the 10-wk
measurement period.

species occurred were used to assess the response of density near the study site censused using the electro-
ramet production to elevated CO2. All data are ex- capture method averaged 150 worms/m2 (see Zaller and
pressed on an areal basis. Nomenclature for plant spe- Arnone 1998).
cies follows Binz and Heitz (1990).
Plant species–cast association
Earthworm community and spatial distribution of
earthworm surface casts To check whether our selection of a 3 3 3 cm cell
On the same 30 3 30 cm grid we also measured size was statistically appropriate for our questions, we
earthworm surface-cast production in each cell every calculated the dispersion index (Krebs 1989) for worm
9 d (see Zaller and Arnone 1997) from 5 April to 19 casts and for each plant species in each 30 3 30 cm
July 1995. Cumulative cast production over this period area in the ambient-CO2 plots. The dispersion index
was calculated for each of the 100 grid cells (Fig. 1 describes whether the spatial distribution of surface
bottom). The overall size of the 30 3 30 cm grid and casts or of an individual plant species, is random, uni-
individual cells were chosen to enable the tracking of form, or aggregated. Goodness-of-fit of each dispersion
individual plants (Huovinen-Hufschmid and Körner index to a random Poisson distribution was tested using
1998) and casts (see below). Individual surface casts chi-square (Zar 1996). We tested cell sizes of 3 3 3
were weighed in the field, and several subsamples from cm, 6 3 6 cm, and 9 3 9 cm. To calculate the plant–
each plot were taken at each sampling date to calculate cast association of each species, we used the cell size
fresh mass/dry mass ratios. After weighing, each cast that produced an aggregated dispersion pattern of that
was slightly deformed (flattened to prevent recounting) plant species and the casts. For 22 of the 28 plant
and returned immediately to its original position in species considered, a 3 3 3 cm cell size was most
order to maintain the natural pattern of cast distribu- appropriate. The remaining six species (four non-leg-
tion. Methodological details of cast sampling are pro- umes, two legumes) would have required larger grid
vided in Zaller and Arnone (1997). sizes than the largest (i.e., 9 3 9 cm) that could be
A total of nine earthworm species was recorded (no- considered in our experiment. Despite this situation we
menclature follows Bouché 1972) near the study site, included all six in the plant species–cast association
representing three ecological groups (Bouché 1977): analyses.
anecics (Lumbricus terrestris L., Nicodrilus longus The degree to which a plant species was associated
Ude., and N. nocturnus Ev.), endogeics (Allolobophora with casts was calculated as the percentage of the total
chlorotica Sav., A. rosea Sav., N. caliginosus Sav., and number of cells in which both that species and casts
Octolasion cyaneum Sav.) and epigeics (Dendrobaena were present divided by the total number of cells in
mammalis Ger. and L. castaneus Sav.). Total earthworm which the plant species was present.
876 JOHANN G. ZALLER AND JOHN A. ARNONE III Ecology, Vol. 80, No. 3

Plant species performance vs. cumulative cast duction and the mass of the associated casts for each
production species and CO2 level. To test for differences in slope
between CO2 treatments, we used two-way ANOVAs
To assess plant species’ growth responses to casts,
(with slopes calculated from the linear regressions for
we took the total number of ramets of each plant species
each plot and species as dependent variables, and CO2
from individuals growing in association with casts in
concentration and block as factors). The final analysis
each 30 3 30 cm sampling area on each plot, and
at the species-within-functional-group level was a two-
plotted this as a function of the total cumulative cast
way ANOVA to test for effects of elevated CO2 on
mass associated with each species (both expressed on
ramet production, with CO2 and block as factors. Anal-
an areal basis). This was done at peak plant community
ogous analyses were conducted at the level of the func-
biomass.
tional group. Nutrient concentrations in casts and ad-
Available nutrients in casts and adjacent soil jacent soil for the two sampling dates were tested using
three-way repeated-measures ANOVAs with CO2,
On 5 June and 11 July 1996, when surface cast pro- block, and substrate type (i.e., cast or soil) as factors.
duction was high, we collected three fresh surface casts All analyses were conducted with plot as the exper-
(not older than 3 d) and adjacent topsoil (to a depth of imental unit. We considered P , 0.05 to be ‘‘signifi-
1.5 cm from areas with no casts present) from each cant’’ and 0.05 ,P , 0.10 to be ‘‘marginally signifi-
experimental plot. Samples from each plot were pooled cant’’. All analyses were performed using SYSTAT
and stored in plastic vials overnight on ice. Material (Wilkinson et al. 1992).
from each vial was mixed and sieved (0.7-mm mesh)
to remove fine roots. To determine ammonium (NH41- RESULTS
N) and nitrate (NO32-N) nitrogen concentrations, 2.0
Plant species association with casts
g of fresh mass was extracted with 20 mL of 2 mol
KCl/L solution by shaking for 1 h. The same procedure Plant species within each of the three functional
was used to extract phosphate-P (PO42-P), except that groups differed significantly in their association with
0.5 mol NaHCO3/L was used as extractant. Filtered earthworm casts at ambient CO2 (Table 1, Table 2a).
extracts were analyzed on a Flow Solution segmented Often plant species that were less abundant were as-
flow analyzer (Perstorp Analytical, Perstorp, Sweden). sociated to a greater degree with casts than were the
NH41-N was determined using the indophenol method more abundant plant species. Mean associations ranged
(Keeney and Nelson 1982). NO32-N was reduced to from 43 to 66% for graminoid species, from 48 to 77%
nitrite (NO22) by Cd then determined using the Griess- for non-legume forbs, and from 8 to 83% for legumes
Ilosvay method (as described in Keeney and Nelson (Table 1). Elevated CO2 had no effect on the degree of
1982). PO42-P was determined using the molybdate- association of plant species with casts within each of
ascorbic acid method (Olsen and Sommers 1982). Sub- the three functional groups (Table 2b). However, non-
samples of fresh cast and adjacent soil were dried at legume forbs and legumes differed in their association
808C to calculate water content and allow expression with casts under ambient and elevated CO2 (i.e., sig-
of nutrient concentration on a dry-mass basis. nificant interactions, Table 2b: P 5 0.036, and P 5
0.081, respectively), with some species exhibiting re-
Statistical analyses ductions and others increases. At the level of the func-
Although we recorded a total of 60 plant species tional group no significant differences were observed
among all 16 A and E plots, our analyses included only in association with casts at either ambient or elevated
those species (28) present on at least two plots per CO 2 CO2 (Table 2a and b).
treatment. To evaluate whether plant species within
Plant species responses to elevated CO2 as a
each of the functional groups differed in their degree
function of association with casts and cumulative
(expressed as %) of association with casts at ambient
cast production
CO2 (n 5 8 replications), we used a two-way ANOVA
with species and block as factors. The effects of ele- Total ramet production was not related to the degree
vated CO2 on plant species–cast association within each that a species, or functional group, was associated with
functional group was tested using a three-way ANOVA casts at either CO2 level (Table 2c). We did, however,
with CO2 concentration, species, and block as factors. see a positive (P 5 0.007, r 5 0.789) relationship be-
All percentage data were arcsin transformed prior to tween the response of graminoid species to elevated
statistical analysis (Sokal and Rohlf 1981). Linear re- CO2 (measured as the percentage change in mean total
gression analysis was used to assess the relationship ramet production of graminoid species, relative to mean
between plant species’ responses to elevated CO2 and total ramet production at ambient CO2) and their mean
the degree of association with casts within each of the degree of association (in percentage) with surface casts
functional groups (using differences of treatment at ambient CO2 (Fig. 2, Table 3). Thus, graminoid spe-
means). We also used linear regression analysis to eval- cies more frequently associated with casts (e.g., An-
uate the relationship between plant species’ ramet pro- thoxanthum odoratum and Carex caryophyllea) pro-
April 1999 PLANT–EARTHWORM INTERACTIONS AT HIGH CO2 877

TABLE 1. Degree of plant species association with earthworm surface casts, and the frequency of plant species in grassland plots
maintained at ambient (Amb., 350 mL CO2/L) and elevated (Elev., 600 mL CO2/L) atmospheric CO2 (data are means 6 1 SE).
Plant species within each of the three functional groups are ranked by their degree of association with casts at ambient CO2.

No. plots†
Plant species–cast assoc. (%) Plant species frequency (%)
Amb. Elev.
Functional group CO2 CO2 Amb. CO2 Elev. CO2 Amb. CO2 Elev. CO2
Graminoids 8 8 56.7 6 2.0 52.5 6 2.9 81.4 6 7.3 90.3 6 2.7
Carex caryophyllea 8 8 65.7 6 8.7 50.7 6 7.8 18.1 6 4.0 29.5 6 5.7
Dactylis glomerata 5 5 65.0 6 8.1 74.3 6 9.8 1.1 6 0.6 2.5 6 0.9
Anthoxanthum odoratum 4 6 64.6 6 3.3 56.5 6 7.1 2.0 6 0.8 5.4 6 1.5
Carex flacca 8 8 58.4 6 4.1 51.8 6 12.1 9.4 6 1.5 12.1 6 3.6
Danthonia decumbens 5 8 56.0 6 6.4 36.3 6 7.2 5.9 6 3.4 5.1 6 1.2
Bromus erectus 8 8 54.8 6 1.7 53.2 6 3.2 61.8 6 2.7 62.1 6 3.3
Cynosurus cristatus 8 6 52.9 6 6.2 50.4 6 11.3 4.5 6 1.0 5.8 6 1.9
Festuca rubra 8 8 52.8 6 10.3 60.4 6 7.9 15.1 6 4.2 8.9 6 1.9
Agrostis tenuis 8 8 52.1 6 1.6 54.5 6 4.6 28.0 6 4.9 25.6 6 4.4
Luzula campestris 6 2 43.3 6 12.9 75.0 6 12.5 2.3 6 0.8 0.4 6 0.3
Non-legume forbs 8 8 59.2 6 2.1 57.7 6 6.2 19.8 6 4.4 18.4 6 3.9
Cerastium fontanum 5 2 76.7 6 11.5 75.0 6 12.5 2.0 6 0.8 0.5 6 0.3
Betonica officinalis 3 3 66.7 6 10.2 22.2 6 13.6 0.9 6 0.5 1.0 6 0.7
Hieracium pilosella 4 3 62.5 6 7.5 25.0 6 12.5 1.3 6 0.6 0.6 6 0.5
Sanguisorba minor 7 7 61.9 6 2.8 59.7 6 8.7 2.1 6 0.7 4.6 6 1.3
Prunella vulgaris 8 7 55.3 6 10.5 57.7 6 9.6 7.8 6 2.2 8.1 6 3.2
Linum catharticum 6 5 52.1 6 4.5 55.0 6 18.1 3.8 6 1.6 1.1 6 0.5
Plantago lanceolata 3 3 50.0 6 5.8 70.0 6 15.8 0.9 6 0.4 1.1 6 0.5
Thymus serpyllum 4 2 50.0 6 17.7 100.0 6 0.0 1.0 6 0.7 0.4 6 0.3
Leucanthemum vulgare 3 3 48.3 6 9.3 83.3 6 10.2 2.0 6 1.3 1.5 6 0.9
Legumes 8 8 55.6 6 9.0 32.9 6 9.3 7.8 6 2.7 5.4 6 1.5
Medicago lupulina 3 2 83.3 6 10.2 75.0 6 12.5 0.5 6 0.3 0.4 6 0.3
Trifolium medium 5 2 66.0 6 14.9 0.0 6 0.0 2.1 6 0.9 0.3 6 0.2
Trifolium spp.‡ 6 6 64.6 6 10.1 40.6 6 13.1 5.5 6 2.3 2.6 6 0.7
Lotus corniculatus 4 5 8.3 6 5.9 20.0 6 9.7 0.9 6 0.4 1.6 6 0.8
† Number of plots where each plant species occurred.
‡ Trifolium spp. include: Trifolium campestre, T. montanum, T. ochroleucon, T. pratensis, and T. repens.

duced more ramets per square meter at elevated CO2 casts increased significantly with increasing cast mass
than those less frequently associated with casts (e.g., in 9 of the 10 graminoid species (Fig. 3), 5 of the 9
Agrostis tenuis and Danthonia decumbens). non-legume forb species (r values ranged from 0.80 to
Total ramet production of species associated with 0.98; P values for linear regression from ,0.001 to

TABLE 2. Results from ANOVAs for (a) differences between plant species–earthworm cast associations at ambient CO2,
(b) effect of elevated CO2 on plant–cast associations, and (c) effect of elevated CO2 on ramet production.

Within functional groups


Between functional groups, FG
Graminoids Non-legume Legumes
Source of Source of
variation df P df P df P variation df P
a) Plant species–cast associations at ambient CO2
Species 9 0.046 8 0.086 3 0.021 FG 2 0.868
Block 7 0.007 7 0.946 7 0.055 Block 7 0.446
Error 49 25 11 Error 13
b) Effects of elevated CO2 on plant–cast associations
Species, Spp. 9 0.020 8 0.160 3 ,0.001 FG 2 0.283
CO2 1 0.162 1 0.851 1 0.188 CO2 1 0.285
Block 7 0.001 7 0.057 7 0.031 Block 7 0.234
Spp. 3 CO2 9 0.347 8 0.036 3 0.081 FG 3 CO2 2 0.498
Error 106 50 18 Error 33
c) Effects of elevated CO2 on production of ramets per m2
Species, Spp. 9 ,0.001 8 0.017 3 0.341 FG 2 ,0.001
CO2 1 0.925 1 0.719 1 0.503 CO2 1 0.807
Block 7 0.916 7 0.069 7 0.630 Block 7 0.588
Spp. 3 CO2 9 0.794 8 0.589 3 0.823 FG 3 CO2 2 0.973
Error 106 50 16 Error 35
878 JOHANN G. ZALLER AND JOHN A. ARNONE III Ecology, Vol. 80, No. 3

DISCUSSION
Our results demonstrate that plant species differ sig-
nificantly in their degree of association with nutrient-
rich earthworm surface casts, regardless of the relative
abundance of plant species in the community. However,
dramatically increased carbon supply to communities
maintained at elevated CO2 (Stocker et al. 1997) did
not affect the degree to which plant species are asso-
ciated with casts (Table 1). Clearly casts had a profound
effect on ramet production for most of the species oc-
curring in the communities when only plants associated
with casts were considered; i.e., increasing total ramet
production with increasing cumulative cast production
per mass (Fig. 3). This effect most likely was due to
higher nutrient availability in larger casts. We and oth-
ers (Springett and Syers 1979, Spiers et al. 1989) have
observed fine-root proliferation into casts, indicating
that plants can exploit these nutrients. Differences in
the abilities of species to exploit these nutrient patches
(sensu Jackson and Caldwell 1992, Bilbrough and
FIG. 2. Response of graminoid species to elevated CO2 Caldwell 1997), especially in the spring when casting
(measured as the percentage change in mean total ramet pro- activity (Zaller and Arnone 1997) and plant growth and
duction of graminoid species, relative to mean total ramet nutrient demand are greatest, may alter the competitive
production at ambient CO2) as a function of their mean degree
of association with surface casts at ambient CO2. Plant species
key: Agr ten 5 Agrostis tenuis, Ant odo 5 Anthoxanthum TABLE 3. Number of ramets for each plant species in plots
odoratum, Bro ere 5 Bromus erectus, Car car 5 Carex car- maintained at ambient (Amb., 350 mL CO2 / L) and elevated
yophyllea, Car fla 5 Carex flacca, Cyn cri 5 Cynosurus cris- (Elev., 600 mL CO2 / L) atmospheric CO2. Plant species
tatus, Dac glo 5 Dactylis glomerata, Dan dec 5 Danthonia within functional groups are ranked by number of ramets
decumbens, Fes rub 5 Festuca rubra, Luz cam 5 Luzula at ambient CO2 (data are means 6 1 SE). See Table 1 for
campestris. See Table 1 for details about individual species details about individual species performance.
performance. The line was fitted by linear regression.
Number of ramets/m2†
Functional group Amb. CO2 Elev. CO2
0.02), and 2 of the 4 legume species across both CO 2 Graminoids 3756 6 203 3762 6 230
treatments (r values ranged from 0.58 to 0.95; P values Bromus erectus 2082 6 173 1988 6 124
for linear regression from ,0.001 to 0.05). However, Agrostis tenuis 647 6 115 518 6 141
Carex caryophyllea 303 6 81 499 6 117
elevated CO2 had no effect on the positive response to Festuca rubra 285 6 91 263 6 75
increasing cast mass (data only shown for graminoid Danthonia decumbens 224 6 134 85 6 22
species; Fig. 3). Carex flacca 125 6 22 163 6 47
Anthoxanthum odoratum 97 6 30 139 6 24
Surface cast production and nutrient concentrations Cynosurus cristatus 75 6 20 96 6 31
Luzula campestris 51 6 10 27 6 6
Cumulative surface cast production measured be- Dactylis glomerata 36 6 12 67 6 19
tween April and August 1995 (as both grams dry mass Non-legume forbs 274 6 76 219 6 48
per square meter and number of casts per square meter) Prunella vulgaris 90 6 27 113 6 42
Leucanthemum vulgare 89 6 51 44 6 17
and average area of soil covered by casts were unaf- Linum catharticum 72 6 31 24 6 8
fected by elevated CO2 (Table 4). The concentrations Plantago lanceolata 39 6 6 15 6 4
of ammonium, nitrate, and phosphate were also not Cerastium fontanum 38 6 10 22 6 0
affected by elevated CO2 in either of the two sampling Thymus serpyllum 37 6 26 17 6 6
Betonica officinalis 30 6 13 37 6 21
dates (NH41-N: P 5 0.470; NO32-N: P 5 0.578; PO42- Hieracium pilosella 28 6 7 33 6 22
P: P 5 0.257). However, per unit dry mass the casts Sanguisorba minor 27 6 8 59 6 14
contained 100% more NH41-N (9.05 6 1.39 mg/g vs. Legumes 86 6 32 53 6 19
4.44 6 0.49 mg/g for casts vs. soil, respectively), al- Trifolium spp.‡ 48 6 28 42 6 9
most 30% more PO42-P (2.27 6 0.20 mg/g vs. 1.79 6 Trifolium medium 44 6 17 17 6 6
0.19 mg/g for casts vs. soil, respectively), but similar Lotus corniculatus 22 6 6 29 6 11
Medicago lupulina 15 6 4 17 6 6
amounts of NO32-N (8.11 6 1.13 mg/g vs. 7.32 6 0.61
mg/g for casts vs. soil, respectively) than adjacent top- † Only plots in which a plant species occurred were in-
cluded in the calculations.
soil, averaged across sampling dates and CO2 treat- ‡ Trifolium spp. include: T. campestre, T. montanum, T.
ments. ochroleucon, T. pratensis, and T. repens.
April 1999 PLANT–EARTHWORM INTERACTIONS AT HIGH CO2 879

FIG. 3. Total ramet production of graminoid species as a function of associated total cumulative surface cast production
in grassland communities maintained at ambient (350 mL CO2 / L; V) and elevated (600 mL CO2 /L; v) atmospheric CO2.
Lines indicate linear regressions across CO2 treatments; results of linear regression analyses across CO2 treatments for each
species are given on the figure. Note varying scales on both axes.

balance among plant species in these communities. The evated CO2 when plants were near larger casts (Fig.
lack of an apparent correlation between cast mass and 3).
ramet (tiller) production of Bromus erectus, the most Although we focused on the role of casts as a nutrient
dominant species in these communities (43% of above- source for plants, other properties of earthworm casts,
ground biomass, Huovinen-Hufschmid and Körner such as possible greater water-holding capacity than
1998), may have been due to its relative inability to neighboring soil (e.g., Edwards and Bohlen 1996), may
respond to nutrient additions (Ellenberg 1986). have contributed to the effects we observed on plants.
The absence of a statistically significant relationship We also cannot rule out the possibility that the presence
between the degree of association with earthworm casts of certain plant species may influence casting patterns.
and responses to elevated CO2 for plant species in any For example, root architecture and distribution have
of the functional groups (e.g., Fig. 2 for graminoids) been shown to influence patterns of earthworm bur-
was puzzling but may simply be due to the fact that rowing (Edwards and Lofty 1980, Springett and Gray
many plant species in these communities had too little 1997), and root exudate quantity and quality may play
time to respond to increased carbon (i.e., elevated CO2; a role in attracting earthworms (Graff 1977). Based on
see also Leadley et al. 1997) and nutrient availability our observations, it also seems that earthworms deposit
(i.e., in casts). Also, the significant (P 5 0.007) positive more casts near plant species with a compact root sys-
correlation between the mean degrees of association tem near the soil surface, and near plant species that
with casts and the mean responses to elevated CO2 of provide some form of shelter to worms (shade, pro-
graminoid species (Fig. 2), indicates that plant species tection from birds) by virtue of their tussock growth
were in fact beginning to respond to both elevated CO2 form (e.g., Anthoxanthum odoratum, Carex spp., Dac-
and increased nutrient availability in the second grow- tylis glomerata, Cerastium fontanum). It should be not-
ing season of CO2 enrichment. Further, cast-associated ed that, although we observed no effects of elevated
ramet production in some species (e.g., Anthoxanthum CO2 on cumulative surface-cast production during the
odoratum, Carex caryophyllea, C. flacca, and Cyno- study period (April to August 1995), we saw a dramatic
surus cristatus) clearly tended to be greater under el- stimulation in subsequent measurements through April

TABLE 4. Cumulative earthworm surface-cast production between 5 April and 5 July 1995 in a calcareous grassland com-
munity maintained at ambient (350 mL CO2 / L) and elevated (600 mL CO2 / L) atmospheric CO2 (data are means 6 1 SE,
n 5 8 replicates).

Cumulative cast production Ambient CO2 Elevated CO2 P†


Dry mass (g/m2) 492 6 4 594 6 58 0.221
Number of casts/m2 999 6 41 1075 6 77 0.484
Plot area covered by casts (%) 58 6 2 60 6 3 0.563
† Effect of elevated CO2; P values are for ANOVA with CO2 level and Block as independent variables.
880 JOHANN G. ZALLER AND JOHN A. ARNONE III Ecology, Vol. 80, No. 3

1996 (Zaller and Arnone 1997). However, it should be Edwards, C. A., and P. J. Bohlen. 1996. Biology and ecology
further noted that the locations of surface cast depo- of earthworms. Third edition. Chapman & Hall, London,
UK.
sition in each 30 3 30 cm grid remained similar up to Edwards, C. A., and J. R. Lofty. 1980. Effects of earthworm
April 1996. inoculation upon the root growth of direct drilled cereals.
Thus, our results demonstrate that (1) plant species Journal of Applied Ecology 17:533–543.
differ significantly in their degree of association with Ellenberg, H. 1986. Vegetation Mitteleuropas mit den Alpen
in ökologischer Sicht. Fourth edition. Verlag Eugen Ulmer,
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Stuttgart, Germany.
relative abundance of plant species in the community— Gavrilov, K. 1963. Earthworms, producers of biologically
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Vegetation und Fauna, Berichte der Internationalen Sym-
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strongly to rising CO2 than those less highly associated skunde. Cramer, Vaduz, Liechtenstein.
with casts; and (3) nutrient-rich earthworm casts stim- Greig-Smith, P. 1983. Quantitative plant ecology. Studies in
ulate the growth (ramet production) of most plant spe- ecology. Volume 9. University of California Press, Berke-
cies in these grassland communities, even at current ley, California, USA.
Grime, J. P., J. C. Crick, and J. E. Rincon. 1986. The eco-
levels of atmospheric CO2. The data further suggest logical significance of plasticity. Pages 5–29 in D. H. Jen-
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ACKNOWLEDGMENTS Huovinen-Hufschmid, C., and C. Körner. 1998. Microscale
patterns of species distribution and biomass in calcareous
We are grateful to: Pascal Niklaus and Paul Leadley for grassland. Botanica Helvetica 108:69–83.
maintaining the CO2-enrichment facility; Christian Körner, Jackson, R. B., and M. M. Caldwell. 1989. The timing and
Stephan Hättenschwiler, and Peter Stoll for valuable com-
degree of root proliferation in fertile-soil microsites for
ments on an earlier version of the manuscript; Dominik Heeb
three cold-desert perennials. Oecologia 81:149–153.
and P. S. for discussions on statistics; and Brigitte Steullet-
Jackson, R. B., and M. M. Caldwell. 1991. Kinetic responses
Müller, Gabriela Hofer, and Gunnar Hirschel for help with
of Pseudoroegneria roots to localized soil enrichment.
cast and soil extractions. This research was supported by
Plant and Soil 138:231–238.
grants from the Swiss National Science Foundation to J. Ar-
Jackson, R. B., and M. M. Caldwell. 1992. Shading and the
none (NF 3100-042401.94/1) and to C. Körner, J. Arnone and
capture of localized soil nutrients: nutrient contents, car-
Bernhard Schmid (NF-SPPU 5001-035214).
bohydrates, and root uptake kinetics of a perennial tussock
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