250 ECOLOGY OF PLANTS
4000 feet. The plants were potted and kept in a cold frame at
Corvallis, Oregon, during two winters after collection so that
all were exposed to the same winter conditions. On February 1
after the second winter, half of the plants from each locality
were placed in a 9-hour photoperiod and half on an 18-hour
photoperiod with all other conditions the same. There were
no effects of photoperiod on time of bud bursting in the low
altitude plants, but the long days hastened bud bursting strik-
ingly in high altitude plants as compared with effects of short
days. The selection probably results from the killing of seed-
lings by low night temperatures at high altitudes if they break
dormancy in the short days of winter or early spring.EFFECTS OF PLANT PRODUCED TOXINSDe Candolle first suggested the existence of naturally-
occurring plant growth-inhibitors in 1832 (Bonner 1950).
He noted from field observations that Euphorbia (spurge)
was apparently inhibitory of flax ( Linum usitatissimum ),
thistles (probably Cirsium ) to oats ( Avena sativa ) and rye
to wheat. Very little research was done on the subject for
almost 100 years at which time Cook (1921) described the
characteristic wilting of potato ( Solanum tuberosum ) and
tomato plants grown near Juglans nigra (black walnut).
Davis (1928) extracted juglone from mature hulls and roots
of black walnut and found it to be very toxic to tomato and
alfalfa ( Medicago sativa ) plants when injected into the stems.
The juglone was identified as 5-hydroxynaphthaquinone.
Proebsting and Gilmore (1940) related the problem of
re-establishing peach ( Prunus persica ) trees in old peach
orchards to the presence of toxic substances in the soil.
Bonner and Galston (1944) reported that the edge rows in
guayule ( Parthenium argentatum ) plantings in California
had much larger plants than the center rows and the differ-
ences could not be eliminated by heavy watering and min-
eral application. Experiments indicated that leachates from
pots of year-old guayule plants were very inhibitory to gua-
yule seedlings. The inhibitor was subsequently identified as
transcinnamic acid.
Muller, Muller, and Haines (1964) observed areas free
of vegetation around certain shrubs in California grass-
lands. They found that at least three shrubs, Salvia leuco-
phylla (clearleaf sage), S. apiana (bee sage), and Artemisia
californica (California sagebush) produced volatile materi-
als which inhibited various test plants. Muller and Muller
(1964) identified several terpenes which were produced by
leaves of three species of Salvia, and two of these, camphor
and cineole, were found to be very inhibitory to test plants.
Muller, Hanawalt, and McPherson (1968) related the disap-
pearance of herbaceous species in the open California chap-
arral during the fire cycle to the production of inhibitory
chemicals by chaparral species.
My students and I have obtained good evidence that the
rapid disappearance of the pioneer weed stage (2 to 3 years)
in our revegetating old-fields in central Oklahoma is due to
the inhibition of seedlings of species of that stage by several
plants of the pioneer stage (Abdul-Wahab and Rice, 1967;Parenti and Rice, 1969; Wilson and Rice, 1968). Triple-awn
grass ( Aristida oligantha ), the dominant of the second stage,
is generally not inhibited by species of the pioneer weed
stage and can grow well in the infertile soil, so it is able to
invade the area.
There is some evidence that antibiotics (substances
produced by microorganisms which inhibit other micro-
organisms) may be important in the growth and distribution
of the higher plants as well as microorganisms. Certain soil
bacteria inhibit the root-nodule bacteria which are important
in adding nitrogen to the soil (Konishi, 1931). Iuzhina (1958)
reported that many soil bacterial, fungi and actinomycetes
are antagonistic to Azotobacter, a free living bacterium that
adds nitrogen to the soil. Some soil microorganisms have
been found to be inhibitory to certain microorganisms that
cause diseases of higher plants (Cooper and Chilton, 1950).
Another level of inhibition is that of microorganisms
against higher plants. There is no question that many, if not
most, pathogenic microorganisms produce abnormal symp-
toms in the host plants through the production of toxins. Very
few of these compounds have been identified and this remains
an important and fruitful field for research. Microorganisms
are sometimes responsible for changing certain non- inhibitory
metabolites of higher plants into inhibitory compounds
(Börner, 1960).
The remaining level of inhibition is that of higher plants
against microorganisms. There is considerable evidence that
resistance of many plants to fungal, viral, and bacterial diseases
may be associated with the production by resistant varieties of
inhibitors of the pathogens (Farkas and Kiraly, 1962; Hughes
and Swain, 1960; Schaal and Johnson, 1955).
Ferenczy (1956) found that the seeds or fruits of 52
species and varieties from 19 plant families contained anti-
bacterial compounds and that seeds of some species were
attacked intensely by molds whereas others were attacked
slightly or not at all. Lane (1965) found that fruits of the
native sunflower, Helianthus annuus, rotted more frequently
during germination tests if certain inhibitors were leached
from them before the tests. Those species in which decay of
the seeds during germination is less likely to occur would
certainly stand a better chance of becoming established.
I have found that many of the low-nitrogen requiring
early plant invaders of abandoned cultivated fields pro-
duce inhibitors of the nitrogen-fixing bacteria (Rice, 1964;
1965b; 1965c). Triple-awn grass, the dominant of the
second stage, is one of the inhibitory species. This would
give such plant species a selective advantage in competition
over plants with higher nitrogen requirements. This prob-
ably slows succession in old-fields, because Rice, Penfound,
and Rohrbaugh (1960) found that the order in which spe-
cies invade revegetating fields in central Oklahoma, begin-
ning with the second stage, is the same as the order based on
increasing nitrogen requirements.
Muller (1965) found that the volatile terpenes from
Salvia leucophylla reduce cell elongation and cell division in
the radicles and hypocotyls of germinating Cucumis sativus
(cucumber) seeds. Muller et al. (1969) reported that two vol-
atile terpenes, cineole and dipentene, which emanate fromC005_001_r03.indd 250C005_001_r03.indd 250 11/18/2005 10:20:12 AM11/18/2005 10:20:12 AM