Release of allelochemical agents from litter, throughfall, and topsoil

Release of allelochemical agents from litter, throughfall, and topsoil

Journal of Chemical Ecology, Vol. 17, No. 1, 1991
RELEASE OF ALLELOCHEMICAL AGENTS FROM
LITTER, THROUGHFALL, A N D TOPSOIL IN
PLANTATIONS OF Eucalyptus globulus
LABILL IN SPAIN
A . M O L I N A , 1 M . J . R E I G O S A , 2'* and A. C A R B A L L E I R A
LCdltedra de Ecolog[a
Facultad de Biologfa
Universidad de Santiago de Compostela
Santiago de Compostela, Spain
~Fisiologfa Vegetal
Dep. Recursos Naturales y Medio Ambiente
Facultad de Ciencias de Vigo. Universidad de Vigo
Aptdo. 874. 36200 Vigo, Spain
(Received June 21, 1990; accepted August 28, 1990)
Abstract--Natural leachates of Eucalyptus globulus (throughfall, stemflow,
and soil percolates) were collected daily during rainy spells in the vegetative
period (February-July), and their effects on the germination and radicle
growth ofLactuca sativa were measured. Concurrently, the effects ofL. sativa
of topsoil and leachates from decaying litter were determined. The results
suggest that toxic allelochemicals released by Eucalyptus globulus may influence the composition and structure of the understory of the plantation and
that this effect is attributable mainly to the decomposition products of decaying litter rather than to aerial leachates. The soil may neutralize or dilute
allelopathic agents, at least below the top few cms.
Key Words--Eucalyptus globulus, allelopathy, Lactuca sativa, natural
leachates, soil, litter.
INTRODUCTION
E. globulus is an exotic species o f e c o n o m i c i m p o r t a n c e in Galicia (northwest
Spain). It often has b e e n i m p l i c a t e d in the degradation o f the e n v i r o n m e n t w h e r e
it has b e e n planted. H o w e v e r , the e c o l o g i c a l m e c h a n i s m s controlling the struc*To whom correspondence should be addressed.
147
0098-0331/91/0100-0147506.50/0
Q t991 Plenum Publishing Corporation
148
MOLINA ET AL.
ture and diversity of a woodland understory are numerous and their individual
effects difficult to distinguish. Any degradation produced by E. globulus is likely
to be due to a group of related stress factors acting synergistically, rather than
to a single well-defined cause.
Several authors (Bellot, 1949, 1966; Castroviejo, 1973; Alvarez and Malvar, 1979) have reported that planting E. globulus over heath decreases the
number of species in the understory as compared with the original heath vegetation. Bara et al. (1985) found that plantations of E. globulus were no lower
in species richness than Pinus pinaster, Castanea sativa, or Quercus robur
plantations, but cover was less and the distribution of life forms different, with
a scarcity of hemicryptophytes and geophytes and a preponderance of tall herbaceous species such as Pteridium aquilinum over heathland species such as
heather and Ulex spp. They suggest that the kind of vegetation beneath E. globulus depends on water use (Diaz Fierros et al., 1982), on the accumulation and
chemical composition of residues (which might give rise to allelopathic phenomena), and on competition for nutrients in poorer soils, and have observed
that E. globulus increased the concentration of exchangeable A1, K, and Mg.
Bara (1970), had found previously that the C : N ratio and acidification tended
to increase in 5- to 12-year-old E. globulus plantations, whereas Guitian (1963)
concluded that E. globulus extracts mobilized more Fe and A1 than those from
Q. robur, thus contributing to the degradation of the surrounding area.
The concurrence of plant species may involve both competition for nutrients
(competition sensu strictu) and allelopathic phenomena in which toxic organic
substances are released into the environment by certain species. The importance
of the latter kind of process in forest ecology, especially in the case of E. globulus stands, has been emphasized by several researchers (Rice, 1974). Arias
(1982) found E. globulus leaves to contain water-soluble and volatile compounds capable of inhibiting the germination and growth of grassland species;
Baker (1966) reported that volatile compounds released by E. globulus suppressed germination and hypocotyl growth in Castanea sativa seedlings but did
not affect E. globulus seedlings. In California E. globulus plantations, Del Moral
and Muller (1969) have shown the importance of fog-drip in the transport and
deposition of foliar metabolites and the potential influence of these metabolites
on the diversity and structure of the understory community. The latter authors
ruled out the possibility that conditions of illumination, nutrient availability, or
soil humidity might suffice to explain the exclusion of grassland species (soil
humidity may even be increased by nocturnal condensation beneath the canopy)
and pointed out that in Australia, where Eucalyptus is native, there are usually
few bushes and fewer grasses in the vicinity of eucalyptus trees.
Other species of the genus Eucalyptus containing soluble and volatile compounds that suppress the growth of grassland species include E. camaldulensis
(Del Moral and Muller, 1970), E. microtheca (A1-Mousawi and A1-Naib, 1975,
ALLELOPATHY IN
Eucalyptus PLANTATIONS
149
1976; A1-Naib and A1-Mousawi, 1976), and E. citriodora (Nishimura et al.,
1984). Del Moral et al. (1978) concluded that foliar leachates of E. baxteri can
prevent the growth of certain heathland shrubs beneath its canopy in its native
habitat and that this is not due to competition. Inhibition of test plants such as
E. viminalis by foliar leachates, radicle exudates, litter, and soil extracts was
also observed in their laboratory. On the other hand, Willis (1980) found that
artificial leachates of green and fallen dead leaves of E. regnans only produced
inhibition at high concentrations.
Chemical analysis of leaves and leachates of E. globulus has revealed a
large number of water-soluble compounds of proven phytotoxic potential,
including the phenolic compounds ellagic, gallic, caffeic, gentisic, p-coumaric,
and chlorogenic acids and the terpenoids cineole, camphorol, and o~-pinene (Hillis, 1966a,b; Del Moral and Muller 1969; Guenther, 1950). Terpenoids can be
phytotoxic at concentrations as low as 1-3 izM (Asplund, 1968), and their effective involvement in allelopathic aggression by Eucalyptus spp. was noted by
Putnam (1983). Trenbath and Fox (1976) reported that E. bicostata leachates
did not contain the terpenoids found in artificial leaf extracts and suggested that
their release into the environment might be brought about by the action of leafchewing insects.
The results discussed above show the allelopathic potential of eucalpytus
trees but do not prove conclusively that allelopathic phenomena actually occur
in plantations. Harper (1977) has emphasized that the techniques traditionally
used for detecting allelopathic processes do not guarantee the validity of results
under field conditions, and Stowe and Bong-Seop (1984) have maintained that
hitherto research on allelopathy has been very extensive but insufficiently intensive. In order to evaluate the importance of allelopathy in a given situation and
to distinguish between laboratory artifacts and genuine plant-plant interactions,
it is necessary to establish a relationship between naturally released products
and observed symptoms of phytotoxicity and to understand the dynamics of the
substances involved.
In this paper we have assessed the phytotoxic potential of natural E. globulus leachates (stemflow, throughfall, and soil percolates) together with the
capacity of the soil for controlling the phytotoxicity of decaying E. globulus
litter.
METHODS
AND MATERIALS
Description of the Site. The source of material was a 23-year-old E. globulus plantation located 250 m above sea level near Santiago de Compostela,
Spain (42~
8~
The plantation faces 218~ with a slope of 26: 100.
The density of the trees is 1289/ha, the average height is 28 m, and the average
150
MOLINA ET AL.
diameter 1.3 m above ground is 22.6 cm. According to the FAO classification,
the soil is a Humic Andosol, although local variations in depth produce areas
of Humic Cambisol with Andic properties. The litter layer is deep and has an
average depth of 35 din, is rich in humic acids, and lies over a reddish brown
transition layer and weathered amphibolite bedrock. The characteristics of the
topsoil (0-20 cm) are listed in Table 1.
The average annual temperature of the area is 12.9~ the average temperature during the coldest month is 5.2 ~ and the average annual precipitation
is 1288 mm, of which only 137 mm fall during the three summer months.
According to Papadakis' classification, the area has a mild maritime thermal
regime and a humic humidity regime (Carballeira et al., 1983). The meteorological data for the period of the study (Figure 1) were obtained from the nearest
weather station (C.S.I.C., Santiago de Compostela) and the rainfall sequence
adjusted to the data obtained from pluviometers located in the proximity of the
plantation.
Leachates, etc., were obtained from a 30 • 80-m plot lying parallel to the
slope and containing 58 trees whose distribution by diameter is shown in Table
2.
Collection of Material. Foliar leachates were collected in 10 randomly
placed PVC pluviometers 1 m deep and 20 cm in diameter. A layer of glass
wool at the bottom of each prevented splashing and retained organic debris that
might otherwise have contaminated the leachate.
Stemflow was taken from 13 randomly chosen trees over 25 cm in diameter
by means of runnels encircling the bole at least three times.
Soil percolates were collected by means of 17 fiat PVC lysimeters 22.5 cm
wide, 50 cm long, and 15 cm deep, which were pushed horizontally into the
soil without damage to its natural structure.
TABLE 1. CHEMICAL CHARACTERIZATION OF ANDOSOL USED
Exchangeable bases
(AcONH4, pH 7) (meq/100 g)
Organic
pH
C (%)
N (%)
C/N
Na
K
Ca
Mg
H20
CIK
8.83
0.76
12
0.50
0.37
0.94
0.43
4.60
4.40
Extractable AI
(C1K) (rneq/100 g)
Extractable acidity
(CI2Ba-TEA, pH 8.2)
(meq/100 g)
Oxalate dithionite extractable
Fe203 (%)
AI203 (%)
0.83
38.92
4.22
5.47
tO
0
L~3
0
E
g l ' 7 . ,H
0
0
0
9
0
LO
0r
ol
~l
o
oI
152
MOLINA ET AL.
TABLE 2. DIAMETER AND HEIGHT OF E.
globulus
TREES
Basal diameter
at 1.3 m (cm)
Height
min-max(m)
Trees %
4.6-15
15-25
25-35
35-45.9
7-29.5
8.5-31.5
25-48.5
39.5-49.5
37
18
26
19
All the above leachates were accumulated over 24-hr periods (9 AM to 9
AM) in opaque plastic bottles, which, like the collectors (pluviometers, etc.),
were washed with distilled water before each collection period. After the amount
collected each day had been measured at the site, samples were rapidly taken
back to the laboratory for assay.
Leachates from decaying litter were obtained by collecting all the eucalyptus material that had fallen in the course of seven days onto randomly located
1-m squares (leaves, bark, twigs, etc.). Thus the material obtained was from
natural abscission; Attiwill et al. (1978) pointed out that the composition of
"artificial litter" obtained by manual abscission differs from "natural litter."
The litter collected was thoroughly mixed to obtain homogeneous samples, and
three samples were taken to determine dry weight at 80~ Thirty-five 30-g
samples then were placed in nylon litter bags of 2 mm mesh. Bocock (1964),
MacCauley (1975), and Gloaguen and Touffet (1980) found no significant differences between rates of decomposition in bags with mesh sizes of 0.5-2.0
and 2.5-5.0 cm. On April 25, the bags were placed in groups of seven at five
randomly chosen points on the site, and one bag was removed from each group
after 1, 15, 30, 60 and 90 days.
Fifteen soil samples of the top 5 cm were taken at random using an auger
5 cm in diameter. Organic material and stones were removed and the sample
was homogenized before assay.
Bioassays. Ideally, the effect of the leachates collected would be tested on
species that are abundant in the vicinity of the plantation but not present in its
understory. However, since all such species germinate and grow slowly and
since it was found that the leachates lose most of their biological activity within
96-112 hr, such bioassays were not feasible. To measure the relative phytotoxic
efficiency of the various natural release mechanisms investigated, we therefore
used Lactuca sativa (var. Great Lakes), a fast-growing species commonly used
in bioassays due to its well-known sensitivity to most phytotoxic substances and
plant growth regulators.
Bioassays of throughfall, stemflow, soil percolates, and litter leachates (see
ALLELOPATHY IN
Eucalyptus
153
PLANTATIONS
below) consisted of sowing 50 lettuce seeds on 3MM Whatman paper in each
of five Petri dishes 10 cm in diameter and wetting them with 7.5 ml of the
leachate being assayed (controls were wetted with water collected in the gauges
placed outside the plantation). In bioassays of soil, the seeds were sown on
3MM Whatman paper laid over 30 g of soil at field capacity. After incubation
in the dark for 48 hr at 24~ and 80% relative humidity, germination rates and
radicle lengths were recorded and the statistical significance of the results was
calculated by means of analysis of variance (Vesereau, 1968).
Litter leachates were prepared by saturating the collected material with
distilled water, allowing it to soak for 24 hr in the dark at 15~
and then
washing with a distilled-water spray until 50 ml of extract per 100 g dry wt had
been obtained, a dilution of 1 : 1. By further dilution with distilled water, 1 : 2,
1 : 10, and 1 : 50 (v/v) extracts were prepared.
In all assays, the pH lay within the range of acidities at which gemaination
and root elongation of L. sativa are not affected (Table 3).
RESULTS AND DISCUSSION
Figure 2 shows that the only date on which the biological activity of foliar
leachates differed from that of water from the control pluviometers at the d =
0.01 level was May 30. Radicle growth was significantly depressed by these
leachates, in which leaf exudate had accumulated on the eucalyptus trees during
six days without rain (see Figure 1). Although there had been 30 days without
rain prior to rainfall on July 9, the amount of rain that fell on this occasion, and
the manner in which it fell, apparently produced greater dilution of the exudates
than on May 30.
Germination was significantly depressed (by over 65%) by samples of
stemflow collected on March 14 and radicle growth was significantly reduced
(by over 66%) by samples collected on July 9 (Figure 3). These dates marked
TABLE3. AVERAGEVALUESANDVARIATIONOF pH IN BIOASSAYEXTRACTS
Rain water (control)
Foliar leachates
Cortical leachates
Edaphic percolates
Soil (pH in water 1 : l v/v)
Litter leachates
Min
Mean
Max
4.3
3.6
3.7
3.7
3.5
3.8
5.1
4.0
3.9
4.1
4.6
4.5
5.8
5.4
4.6
4.7
4.9
5.0
154
MOLINA
ET
30--
AL.
LS.D
20_
o
....
0--
o~ - 1 0 _ _
o
:~ - 2 0 _
m
0C - 3 0 - -
nl
i .........
....................
. . . .
_11 .........
20_
o
10_
-
0_
u
rl
i-1
n
i-1
rl
r~
20--
--1'~
rn m40_
= 30-m
-::
r 20-m
o 10--
I
113
I
,
I
1~
I
115
i
I
I
116
i
117
Ti me
FIG. 2. Effects of natural foliar leachates from E. globulus on seed germination and
linear growth of radicles of Lactuca sativa. (Results expressed as % of control values.
Dashed line indicates LSD from control at 1% level of significance.)
the ends of the longest exudate accumulation periods (15 and 31 days, respectively).
The above results suggest that aerial leachatcs are not a significant source
of allelochemical agents unless a set of fairly infrequent conditions coincide.
Toxins must accumulate (Figure 4) during a long rainless period without leaching, and their allelopathic effects also depend on the quantity of rain falling,
the duration of the rainfall, and on the phenological state of the plant (Mitchell,
1968; Tukey, 1969; Turner and Quarterman, 1975; Squires and Trollope, 1978).
Figure 4 shows the height of the electrolyte concentration in the leachates after
light rainfall.
Soil percolates (Figure 5) exhibited relatively little biological activity when
compared with that of topsoil (Figure 6). Germination was unaffected, and radicle growth was only inhibited by soil leachates collected on April 18 and July
7, when the concentration of allelochemicals was high in the first leachate after
long periods without rain.
Topsoil (Figure 6) had no significant effect on germination levels, but
severely reduced radicle growth (up to 70% reduction, compared to controls).
The three inhibition maxima coincide with the ends of the longest rainless
periods of exudate accumulation (31, 10, and 8 days, ending on July 7, June
16, and May 30, respectively). Phytotoxicity increased notably as the summer
ALLELOPATHY
~o__
2
_ 1o--
cc
-20--
Eucalyptus P L A N T A T I O N S
155
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
20-c
2
IN
h
o_
n
o
u -
j%
nn
-
U
""
~1
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
--i
]'~
20,-18_
.O-E
o ~3Q_
c
20--
"~.
-30--
r,
-40__
Wtree
o
5--
;-
L
I
,
I
lj3
,
I
1]4
I _1
I
t15
116
117
Time
FIG. 3. Effects of natural cortical leachates from E. globulus on seed germination and
linear growth of radicles of Lactuca sativa. (Results expressed as % of control values.
Dashed line indicates LSD from control at 1% level of significance.)
m. m h o s
200_
150I00-
50~
S
t
e m flow
percolate
'CONTROL
O
5
10
15
30
(Rain f a l l
outside plantation}
I/ m 2
(I/tree)
FIG. 4. Relationship between conductivity and leachate concentrations.
156
MOLINA ET AL.
2O--
_1%
10__
orl
o_~
Pl
,,
U JJ_
-lO_
-20__
u
J%
- 30--
r~
-40 10__
t-i
Z
-10_
~
mm
|
U
n
n
U
u
__1%
3--
,I,
5
i
114
115
!
117
116
Time
FIO. 5. Effects of natural topsoil percolates from E. globulus on seed germination and
linear growth of radicles of Lactuca sativa. (Results expressed as % of control values.
Dashed line indicates LSD from control at 1% level of significance.)
o--
I0--
-2O--
~
-30--
40__
~
Q:
5O--
Z
-60-20__
rlri
0
.
.
rl
.
113
.
.
o
LT.
.
.
.
114
.
.
.
.
.
.
1~5
.
.
.
.
.
.
.
~
.
.
.
.
.
116
.
.
.
.
.
.
~.
117
T i me
FIG. 6. Effects of soil (0-5 cm) from E. globulus on seed germination and linear growth
of radicles of Lactuca sativa. (Results expressed as % of control values. Dashed line
indicates LSD from control at 1% level of significance).
progressed, possibly due to variation in the quantity or nature of decomposing
litter (Figure 8 below), acceleration of decomposition and toxin release due to
higher temperatures (Molina et al., 1984), or changes in the phenology of the
trees, the activity of soil microorganisms or water and redox potentials.
Figure 7 shows the germination and radicle growth bioassay data analyzed
ALLELOPATHY IN
Eucalyptus PLANTATIONS
157
%
.&.
100
L
Radicle ~en,q t h
~------,...~
Germination
50
1:10
1:50
%
1:21:1
Concentration
1O0
Radicle length
[
B
50
I L. O.
0
1's
I
ao
n
4s
~o o.ys
FIG. 7. Effects of natural litter leachates from E. globulus on seed germination and
linear growth of radicles of Lactuca sativa. Split-plot analysis for leachates concentration (A) and time (B). (Results expressed as % of control values. Dashed line indicates
LSD from control at 1% level of significance).
by a two-way analysis of variance, which showed no interaction. LSDs were
calculated in two one-way analyses of variance. Germination was depressed by
all the leachates prepared, but radicle growth was significantly decreased only
by leachates 1 : 1 and 1 : 2. The maximum reductions in both germination levels
and radicle growth were about 50%. Maximum toxicity was exhibited between
15 and 45 days after abscission, and leachates 1 : 1 and 1 : 2 still caused severe
inhibition after 90 days, even though toxins should have leached out of the litter
on site during this period. Leachates 1 : 10 and 1 : 50 depressed radicle growth
up to day 30 and germination up to day 60. In assessing the significance of
these results, it should be borne in mind that the total quantity of litter falling
during the period covered by the study was well over 400 dry wt/m 2 (Figure
8), making the concentrations of the extracts bioassayed well within the concentration range that might be expected under natural conditions. Eucalyptus
trees are peculiar in shedding litter continually, so that the release of toxic
leachates from decaying litter occurs year-round. Most litter falls just before
158
MOLINA
dwlm~
6L
50__
4L
30-20__ %
10-- ~
O--
ET AL.
/Leaves
/
//•t
/
\\
\
I
\
~\
"
~'"~
.......
~I.
,15
"
"~
.......
......,.Flowers
. . . . . . . . . . .
,16
lb
+ Frui ts
"Branches
Time
FIG. 8. Litter fall components of E. globulus over the study period.
the summer (Reichle, 1981), not in autumn as in the case of native species such
as Quercus robur, thus circumventing the defensive strategies of native understory species.
The above results indicate that the most important mechanisms by which
eucalyptus toxins are released into the soil are through the decomposition of
fallen litter. Some seemingly contradictory findings should be noted, however.
First, in the present study the high inhibitory activity of both litter leachates
and topsoil were washed away by rainfall, whereas the contrary was observed
by Becker and Drapier (1985) in Abies alba Mill. plantations. Second, litter
leachates are more toxic than soil or soil percolates (although the loss of toxicity
by the percolates may have been due merely to their already being diluted when
collected). Third, and most strikingly, while litter leachates mainly depress germination, topsoil reduces radicle growth.
The processes in the soil to which allelochemicals released by plants are
subjected are complex and largely unknown and may result in either synergistic
or antagonistic effects (Rice, 1974; Kaminsky, 1981). Possible interactions
include the breakdown of active compounds after absorption by soil colloids
and the induced release from colloids of growth promotors, which might compensate for the inhibition caused by the eucalyptus toxins. Such promotors might
proceed either from other species in the community or from microbial synthesis.
Without a doubt, the allelopathic effects of E. globulus on the decomposition
and structure of its own understory can only be fully elucidated by means of a
thorough biochemical study of the soil, including its microflora and mycorrhizae. The interaction between direct and indirect allelopathic processes, and
between these processes and water availability, pathogenic agents, the perturbation of nutrient uptake and ionic toxicity must all be considered. The present
results, nevertheless, demonstrate that the chief mechanisms for the release of
ALLELOPATHY IN Eucalyptus PLANTATIONS
159
allelochemicals by E. globulus is the decomposition of litter and that the toxicity
of the litter is especially effective during the delicate establishment stage of the
target species. This would explain the paucity of the understory, when compared with nearby groups of trees of other species, and might also affect the
balance among different life forms (Bara et al., 1985).
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