Vol. 57, No. 1
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Jan. 1991, p. 19-28
0099-2240/91/010019-10$02.00/0
Copyright © 1991, American Society for Microbiology
Influence of the Size of Indigenous Rhizobial Populations on
Establishment and Symbiotic Performance of Introduced
Rhizobia on Field-Grown Legumest
JANICE E. THIES, PAUL W. SINGLETON, AND B. BEN BOHLOOL*
University of Hawaii, NifTAL Project, 1000 Holomua Avenue, Paia, Hawaii 96779-9744
Received 1 August 1990/Accepted 14 October 1990
Indigenous rhizobia in soil present a competition barrier to the establishment of inoculant strains, possibly
leading to inoculation failure. In this study, we used the natural diversity of rhizobial species and numbers in
our fields to define, in quantitative terms, the relationship between indigenous rhizobial populations and
inoculation response. Eight standardized inoculation trials were conducted at five well-characterized field sites
on the island of Maui, Hawaii. Soil rhizobial populations ranged from 0 to over 3.5 x 104 g of soil-1 for the
different legumes used. At each site, no less than four but as many as seven legume species were planted from
among the following: soybean (Glycine max), lima bean (Phaseolus lunatus), cowpea (Vigna unguiculata), bush
bean (Phaseolus vulgaris), peanut (Arachis hypogaea), Leucaena leucocephala, tinga pea (Lathyrus tingeatus),
alfalfa (Medicago sativa), and clover (Trifolium repens). Each legume was (i) inoculated with an equal mixture
of three effective strains of homologous rhizobia, (ii) fertilized at high rates with urea, or (iii) left uninoculated.
For soybeans, a nonnodulating isoline was used in all trials as the rhizobia-negative control. Inoculation
increased economic yield for 22 of the 29 (76%) legume species-site combinations. While the yield increase was
greater than 100 kg ha-' in all cases, in only 11 (38%) of the species-site combinations was the increase
statistically significant (P < 0.05). On average, inoculation increased yield by 62%. Soybean (G. max)
responded to inoculation most frequently, while cowpea (V. unguiculata) failed to respond in all trials.
Inoculation responses in the other legumes were site dependent. The response to inoculation and the
competitive success of inoculant rhizobia were inversely related to numbers of indigenous rhizobia. As few as
50 rhizobia g of soil-' eliminated inoculation response. When fewer than 10 indigenous rhizobia g of soil-'
were present, economic yield was significantly increased 85% of the time. Yield was significantly increased in
only 6% of the observations when numbers of indigenous rhizobia were greater than 10 cells g of soil-'. A
significant response to N application, significant increases in nodule parameters, and greater than 50% nodule
occupancy by inoculant rhizobia did not necessarily coincide with significant inoculation responses. No less than
a doubling of nodule mass and 66% nodule occupancy by inoculant rhizobia were required to significantly
increase the yield of inoculated crops over that of uninoculated crops. However, lack of an inoculation response
was common even when inoculum strains occupied the majority of nodules. In these trials, the symbiotic yield
of crops was, on average, only 88% of the maximum yield potential, as defined by the fertilizer N treatment.
The difference between the yield of N-fertilized crops and that of N2-fixing crops indicates a potential for
improving inoculation technology, the N2 fixation capacity of rhizobial strains, and the efficiency of symbiosis.
In this study, we show that the probability of enhancing yield with existing inoculation technology decreases
dramatically with increasing numbers of indigenous rhizobia.
Inoculation of legumes with exotic strains of rhizobia is a
common agricultural practice intended to promote nitrogen
fixation and increase crop yield. Despite improvements in
inoculation methods (3, 13, 31, 34) and selection of rhizobial
strains for increased nitrogen fixation capacity (16), compet-
itive ability (1), and ability to withstand environmental stress
(15, 17, 19), inoculation does not always lead to increased
plant growth and crop yield.
Plant response to inoculation is determined by a variety of
factors. The presence and quality of indigenous rhizobial
populations (3, 6, 11, 27), soil nitrogen (N) availability (9,
32), soil physicochemical constraints (12, 24), and climatic
conditions (4) all significantly influence the ability to achieve
increased crop yield through inoculation.
Population density, effectiveness, and competitive ability
are the primary characteristics of indigenous rhizobial pop-
*
Corresponding author.
t Journal series no. 3494 of the Hawaii Institute of Tropical
Agriculture and Human Resources.
ulations that affect inoculation responses.
In
greenhouse
studies, Singleton and Tavares (27) demonstrated that sta-
tistically significant inoculation responses can be eliminated
when there are as few as 20 indigenous rhizobia
g
of soil-' as
long as the population contains some effective strains.
Strains within populations of rhizobia differ
significantly
in
their ability to supply the host plant
with fixed N
(effective-
ness) under greenhouse conditions (24, 26, 27).
Differences
in the effectiveness of inoculant strains can also be demon-
strated under field conditions as
long
as the soil is free of
indigenous rhizobia (10). In the
presence
of an
indigenous
population, however, improved crop yield through
inocula-
tion with more effective inoculant strains is difficult to
demonstrate (6, 11, 18).
Successful competition for nodule sites
by indigenous
rhizobia is one reason for the failure to achieve a
response
to
inoculation with elite rhizobial strains
(18, 36).
Both
pot
experiments (2) and field trials
(36)
demonstrated that to
achieve nodule occupancy of
greater
than
50%,
inoculant
rhizobia must be applied at a rate at least
1,000
times
greater
19