OFFPRINTS FROM INTEGRATED PEST MANAGEMENT SYSTEMS AND COTTON PRODUCTION, IED
Edited by Raymond E Fnsbie. Kamal M El-Zik. and L Ted Wilson
Copyright O 1989 by John Wiley & Sons. Inc
7
BIOLOGICAL CONTROL OF
PEST POPULATIONS
I
W . L. Sterling
~
Department of Entomology
Texas A&M University, College Station, Texas
K . M . El-Zik
Department of Soil and Crop Sciences
Texas A&M University, College Station, Texas
L. T . Wilson
Department of Entomology
University of California, Davis, California
Natural Control of Arthropod Pests
Current Practices in Cotton Arthropod Management
Nonintervention as a Tactic
Key Predators
Inaction Levels
Natural Control of Selected Arthropod Pests
Boll Weevil
Heliothis spp.
Cotton Flea hopp er
Lygus Species
Pink Bollworm
Spider Mites
Other Pests
Arthropod Control with Microbials
155
156
Biological Control of Pest Populations
Natural Control of Plant Pathogens
Concepts and Mechanisms
Approaches to Biological Control of Cotton Pathogens
Current Status of Biological Control of Plant Pathogens
Natural Control of Weeds
Toward Classical Biological Control
Augmentation of Natural Enemies
Restoration Ecology
Classical Biological Control
Conclusion
References
In this chapter biological control is defined as applied natural control. Thus
any way that man intervenes to improve the efficacy of the natural enemies
of pest species, whether by introductions, conservation, or augmentation,
is classified as biological control. Suppression, maintenance, or regulation
of organisms by natural enemies or the physical environment in the absence
of human intervention to manipulate them constitutes natural control.
The following sections cover the biological control of arthropods, plant
pathogens, and weeds. For the arthropod sections, emphasis is placed on
naturally occurring predators, with no intent of minimizing the importance
of naturally occurring parasites, pathogens, or physical mortality. Although
less developed in cotton, we provide evidence recognizing the importance
of natural enemies in effecting the regulation of pathogen and weed pests.
NATURAL CONTROL OF ARTHROPOD PESTS
The total complex of natural enemies, including predators, parasites, and
pathogens, plays an important role in preventing most potential arthropod
pests in most cotton-growing regions of the United States from causing economic loss. Native natural enemies usually dominate the dynamics of most
pests, so that management intervention is rarely needed to prevent economic
losses. Exceptions include certain key, induced, or occasional pests that
temporarily escape control, or induced pests in agroecosystems continuously
perturbed with agrichemicals. The boll weevil (Anthonomus grandis) and
the pink bollworm (Pectinophora gossypiella), which have few effective
natural enemies in some parts of the United States, may be exceptions in
cotton agroecosystems.
Some of the initial evidence supporting the foregoing statement was provided by examples of natural enemy perturbations with insecticides. For
example, in the San Joaquin Valley of California, the treatment of Lygus
?
Natural Control of Arthropod Pests
157
with organophosphate insecticides had a severe impact on the natural enemies that normally keep Heliothis spp., beet armyworm, and cabbage loopers in check (Falcon et al., 1971; van den Bosch and Hagen, 1966). In the
absence of natural enemies, populations of these pests build rapidly. During
the late 1960s and early 1970s, San Joaquin Valley cotton received as many
as 6 to 14 sprays per season, with most treatments directed at bollworm.
This scenario has been repeated in Peru (Smith and van den Bosch, 1967),
Western Australia (Sterling, 1984), south Texas (Adkisson, 1971), Egypt,
Mexico, and South and Central America (van den Bosch, 1978), and
will probably be repeated whenever unilateral insecticidal panaceas are
attempted.
In the past, treatments of insecticides for the control of boll weevil and
fleahoppers have decimated natural enemies of the bollworm and the tobacco
budworm, resulting in tremendous outbreaks in Texas (Adkisson, 1973).
Where insecticidal control of the boll weevil or fleahopper is avoided in early
or midseason, widespread outbreaks of the bollworm and budworm seldom
occur, and they may be relegated to the status of secondary pests.
Current Practices in Cotton Arthropod Management
Native natural enemies and other natural control factors are primarily responsible for the control of cotton insect pests in Texas, in California, and
probably in most other cotton-growing regions where they are not decimated
by repeated applications of broad-spectrum insecticides. For example, using
the most recent data available, 66% or 2.28 million acres of the cotton
acreage in Texas received no foliar applications of insecticides in 1983
(Anon., 1985). Cotton on 1.13 million acres received 2.6 foliar applications,
and 1.12 million acres received 1 seed application in 1983. The overlap between acres treated with foliar or seed application is not known. Conservatively assuming that each application of insecticide has some residual
efficiency for 7 days, the foliar-treated acres are protected by insecticides
for about 19 days during the growing season. It is assumed that seed treatment provides some protection from insect pests for 14 days after emergence.
Based on these data and assumptions, we calculate that about 95% of the
time, cotton in Texas is growing essentially free of insecticides and is depending on the natural control of pests (Table 7.1). Similar statistics are
available for California, where an average of between 1 and 2 sprays are
applied annually, in addition to 50% of the 0.9 to 1.3 million acres also
receiving a prophylactic insecticidal seed treatment. Absence of pests in a
cotton field may also be attributed largely to natural control of the pests on
their reservoir host plants.
The data provided in Table 7.1 are based on the best estimates of several
extension personnel from different areas of Texas. It seems fair to conclude
that a majority of cotton in Texas and California is grown using a “low input”
system where chemical insecticides are used infrequently or not at all. On
158
Biological Control of Pest Populations
Table 7.1 Comparison of Cotton Growing Season (1983) When the Crop Was
Protected by Chemicals (CHEM) as Compared to Protection by Natural Control
“T)
Acres
Treatment
( x lo6)
Foliar
Seed
Untreated
1.13
1.12
2.28
Average
Treatments
Cumulative
Acres
2.6
1.o
2.98
1.12
2.28
0.0
Days
Days
Percent
CHEM
NAT
NAT
19
14
141
146
160
88
91
O
100
95.2
the other hand, some growers choose a “high input” system and may use
15 or more applications of insecticides during the growing season. Growers
that spray frequently for cotton insect pests tend to prescribe to the notion
that they are minimizing the risk of insect damage by using insecticides rather
than by depending on natural control. Other growers, who use limited
amounts or no insecticides, apparently feel that it is to their advantage to
depend on natural control. It is likely that exclusive dependence on either
insecticides or natural enemies is not the optimal solution to all pest problems. Sometimes too few natural enemies are available to control outbreaks
of pests. On the other hand, to use insecticides when they are not needed
is also not optimal. Growers who lean toward insecticidal solutions will tend
to spray when in doubt, whereas growers who lean toward natural control
solutions may tend to refrain from spraying when in doubt. Both groups of
growers are probably making erroneous economic and ecological decisions
on occasion. What is needed is a means of increasing the confidence of
decisions made regardless of the propensity of growers to chose one strategy
over the other. Before growers can make decisions with confidence, the
efficacy and impact of natural enemies must be highly predictable. To be
able to predict their impact, it is essential to know which natural enemies
are the most important and how many are needed to control pest populations.
Nonintervention as a Tactic
It is clear from the discussion above that if cotton is not being protected
by chemicals during 95% of the growing season, the dominant decision being
made by the growers is not to intervene in the affairs of natural enemies or
pests in cotton fields. Often, the best decision that a farmer can make is to
do nothing about the pests except to let the natural enemies do their job.
The key decision is to determine whether there is an economic and environmental justification for intervening in the affairs of predators, parasites,
or pathogens as they go about controlling pests.
Key Predators
If we are to take maximum advantage of natural enemy
Natural Control of Arthropod Pests
159
species as control agents, the effective species should be identified and some
quantitative measure of their efficiency must be established (Roach et al.,
1979). This information should greatly aid in our ability to predict the numbers of pests. Any predator species or stage of a predator species that provides predictive value for forecasting future prey population trends and is
capable of providing irreplaceable mortality leading to prey population control may be considered a key predator (Sterling, 1984). Irreplaceable mortality is the fraction of the total generation mortality attributed to one natural
enemy species so that pest (or prey) survival would increase significantly if
the natural enemy species were removed from the ecosystem. An example
of irreplaceable mortality (Fig. 7.1) is provided by the ants, Solenopsis invicta, a key predator of the boll weevil. When ants were selectively removed
with Mirex insecticide, boll weevil numbers increased dramatically during
both 1974 and 1978.
Removal of a secondary predator would probably have little noticeable
impact on prey abundance. Since.over 600 species of predaceous arthropods
inhabit cotton fields (Whitcomb and Bell, 1964), it is intuitive that most do
not contribute measurable irreplaceable mortality to any particular prey.
Definitive evidence supporting the classification of the key predators inhabiting cotton agroecosystems is largely lacking. However, based on available data, estimates have been provided as to those predators that probably
satisfy the criterion of a key predator (Johnson et al., 1986; McDaniel and
Sterling, 1979,1982; Ridgway and Lingren, 1972; Sterling et al., 1984; Wilson
and Gutierrez, 1980).
The treatment of various predaceous arthropod species as if they were
equal in effectiveness cannot be justified any more than expecting various
pest species to have an equal impact on cotton yield. Each species and
developmental stage has a different prey preference, searching rate, response to prey density, and feeding rate. Although there is some pragmatic
justification for “collapsing natural enemy impact information to a common
unit” (Tamaki et al., 1974; Wilson, 1985), the predictive value of such units
is limited by the degree of realism in the relative weightings assigned to each
predator species and age class (Hartstack and Sterling, 1986, 1988). To simplify the complexity of dealing with multiple species, Hartstack et al. (1975)
suggested that key predators be identified and then treated as independent
units in predictive computer models. We discuss these concepts further later
in the chapter.
Inaction Levels The density of natural enemies sufficient to maintain
pests below the action level (economically damaging levels) is the definition
of an inaction level (Fillman and Sterling, 1985; Sterling, 1984). The establishment of inaction levels for natural enemies is suggested as one of the
first steps in optimizing pest management decisions so that the impact of
mortality factors that impinge on pests can be considered. Management decisions based solely on the abundance of pests can result in unneeded ex-
Biological Control of Pest Populations
160
EFFECT OF ANT REMOVAL
100
-+- ANTS REM
+ W/ANTS
/
80
8
IR
n
3
/
60
n
w
0
4
3
40
a
R
20
/
0
2
0
0
2
2
1
0
c3
cv
N
DAY OR YEAR (1974)
EFFECT OF ANT REMOVAL
-+- ANTS REM
-9-
140
150
160
170
180
W/ANTS
190
DAY OF YEAR (1978)
Figure 7.1 Impact of ants on boll weevil populations. After Jones and Sterling (1979) and Sterling
et al. (1984).
Natural Control of Arthropod Pests
L
I
1
0.8
1
.
1
I
161
I
1
TOTAL
MORTALITY
0.6
0.2
hzbv
1PARAS1T I SM
0.1
0
I
-
I
,k2
-
DESICCATION
-*-
0-•
0.1 -
.-
4
E G G INFERTILITY
1
.
L.
\u-*-*\
I
2
3
4
5
6
I
7
8
9
WEEK
Figure 7.2 Impact of four mortality factors on the boll weevil. After Fillman and Sterling (1983).
penses for chemical insecticides and harm to the environment. If sufficient
numbers of natural enemies are present to control the pests, decisions to
use either insecticides or inundative releases of biotic mortality agents would
not be cost-effective.
Natural Control of Selected Arthropod Pests
Boll Weevil Although the boll weevil has many natural enemies (Hinds,
1907; Hunter and Pierce, 1912), the impact of these enemies on the dynamics
of the boll weevil is generally unknown. One exception is the impact of red
imported fire ants. The inaction level of red imported fire ants needed to
limit boll weevil abundance has been determined for conditions in east Texas.
A density of 0.4 ant per plant terminal will provide boll weevil control about
90% of the time (Fillman and Sterling, 1985). Expected mortality rates over
a range of ant densities provides a continuum of inaction levels for use when
the impact of other mortality factors, including desiccation, parasitism, disease, and egg inviability, are available. The evidence indicates that in some
locations the red imported fire ant functions as a key predator (Fig. 7.2) of
the boll weevil (Fillman and Sterling, 1983).
Methods useful in the assessment of boll weevil mortality occurring in
the flower buds have been detailed by Agnew and Sterling (1981), Fillman
Biological Control of Pest Populations
162
3.5
COMPARISON OF CONTROL TACTICS
CHEMICAL
&9 NATURAL
3
s
\
0
W 2.5
J
c
m
z
a
2
J
6.4
2
1.5
1
71
72
73
74
76
77
78
79
80
81
82 AVG
YEAR
Figure 7.3 Comparison of chemical and natural control for the boll weevil during 11 years in
east Texas. After Sterling et al. (1984).
and Sterling (1983), Sterling (1978), and Sturm and Sterling (1986). The major
advantage of their methods is that the developing weevils in the decaying
flower buds or green bolls remain undisturbed and are not removed from
their natural habitat until all mortality factors have had an impact on the
preemergent boll weevils. Using the evidence remaining with the flower bud
or green boll, age-specific mortality from both biotic and physical causes
can be reliably identified, the exception being that mortality of free-living
adults is not measured. However, identification of 98% of the seasonal cohort
mortality was possible during 1981 using these methods (Fillman and Sterling, 1983). On the average, only 2% of each generation survived to the freeliving adult stage. Sterling et al. (1984) provided evidence supporting the
effectiveness of natural enemies, especially ants, in regulating boll weevil
abundance. In an east Texas cotton field, natural control of boll weevils
resulted in higher yields than insecticidal control in 7 out of 11 years due
primarily to mortality attributed to ants (Fig. 7.3).
Contemporaneous mortality (sensu Morris, 1965; Royama, 1981) can
sometimes confuse the assignment of mortality to a single agent. The most
commonly observed example of contemporaneous mortality in boll weevil
studies has been parasitization by Bracan mellitor and predation by the red
imported fire ant. The issue of contemporaneous mortality is confused when
the evidence of parasitization is removed by the ant predator. The presence
of a parasite cocoon in the old boll weevil pupal cell constitutes acceptable
evidence of parasitism. However, when the ants remove the immature boll
Natural Control of Arthropod Pests
163
weevil, they may also remove the parasite pupal cocoon. Thus the incidence
of parasitism may often be underestimated when using durable evidence
techniques. But the total generation mortality will not be underestimated if
contemporary mortality exists. This is an example of replaceable mortality,
that is, the boll weevil mortality attributed to either the parasite or predator
was replaceable since boll weevils not killed by ants would have been killed
by parasites, and vice versa. Of course, both ants and parasites kill some
boll weevils that would have otherwise survived, and thus either one has
the potential to contribute irreplaceable mortality. Ant predators that kill
parasites when feeding on the weevil are viewed as a potential threat to both
native and introduced parasitoids (Cate, 1985). However, since no introduced natural enemy of the boll weevil has become permanently established
in the United States (Cate, 1985), and since the potential for classical biological control of pests of annual crops is low (Simmonds, 1948), the threat
of ants to parasitoids may be more of a theoretical interest than of a practical
one.
It is generally thought to be far safer in empirical studies to find ways to
evaluate the causes of mortality than to depend entirely on correlative data
based on samples of natural enemy and pest abundance. Thus greater confidence is possible where evidence of the mortality of each individual animal
is obtained rather than from extrapolations of population density studies. At
the risk of redundancy, the often-quoted admonition that “correlation is not
causation” is still appropriate. But we would add that correlative evidence
of causation can add increasing confidence to observations of mortality to
individual animals. Using both experimental methods should provide more
definitive evidence than either one alone if they lead to the same conclusion.
Heliothis spp. In the absence of natural enemy-induced mortality, P. M.
Ives and L. T. Wilson (unpubl. data) recorded about 60 to 70% of Heliothis
mortality before reaching the more damaging fourth and fifth larval instars.
This level of mortality, although substantial, is not sufficient to prevent Heliothis from reaching damaging levels. Natural enemies in combination with
physically induced mortality have been observed to contribute up to 100%
mortality of the egg and first two larval stages under field conditions
(McDaniel et al., 1981; Wilson and Gutierrez, 1980). In just 2 days, Heliothis
eggs exposed to native natural enemies experienced an average of 86.6%
daily mortality from eight weekly experiments (McDaniel and Sterling,
1982). Losses to cotton from damage inflicted by Heliothis were low when
such high levels of mortality were observed. In fact, at this high level of
mortality, Heliothis was not even surviving at replacement levels (Le., Ro
< 1). Similar high levels of mortality have been observed by others (DeLoach
and Peters, 1972, Fletcher and Thomas, 1943; van den Bosch et al., 1969).
Under laboratory conditions, female Heliothis will on average produce
between 370 and 1774 eggs, the number depending on the species and temperature conditions (Fye and McAda, 1972). Assuming that an average of
164
Biological Control of Pest Populations
Table 7.2 Cumulative Percent Mortality of Bollworm Immatures to the End of Each
Stage, Shafter, California, 1974
Instar
Date
1
2
3
4
5
n
87.6
89.8
96.3
100
100
1674
3965
2675
2958
1669
~~
6/18-28
718- 1 1
7/26-29
8/18-21
916- 11
67.5
82.7
89.9
95.4
>99
Source: Wilson et
84.1
87.0
94.0
>98
100
85.5
88.6
96.0
100
100
87.0
89.1
96.1
100
100
al. (1980).
1000 eggs are produced per female under field conditions, and for the sake
of argument that the large majority of the mortality occurs prior to or following the reproductive period (fairly realistic assumptions), 99.9% mortality
would be necessary to maintain the population below a replacement level.
In field experiments Wilson et al. (1980) reported preadult mortality levels
reaching 100% during the boll maturation period of crop growth (Table 7.2).
Prior to that period, when mortality levels were less, in some cases the
compensatory nature of cotton allowed for extreme levels of damage with
no resultant effect on crop yield or quality (Wilson and Bishop, 1982).
Augmentation of predators has been demonstrated to reduce Heliothis
spp. up to 90 to 99.5% (Lingren et al., 1968; Lopez et al., 1976; Ridgway
and Jones, 1968). These statistics demonstrate the capacity of natural enemies to control Heliothis spp. Other studies provided lower estimates of
natural enemy efficacy, but these studies generally underestimated total generation mortality because mortality for all prey ages was not measured. For
example, predation accounted for only an average of 24% loss in Texas over
a six-year period when only egg mortality was observed (Fletcher and
Thomas, 1943). A review of published evidence of Heliothis egg and larval
natural control led Ridgway and Lingren (1972) to conclude that from 50 to
90% mortality per generation can be expected and an average of 75% might
be a reasonable average. However, average values such as this can be of
little aid in making pest management decisions, since for any one cotton
field the level of natural control may range from 0 to 100% for any particular
pest population.
Predators of Heliothis that may qualify for the designation of “key predator” include the pirate bugs (Orius spp.), big-eyed bugs (Geocoris spp.),
fire ants (Solenopsis spp.), green lacewings (Chrysopa spp.), cotton fleahoppers (Pseudatomoscelis seriatus), black and white jumping spiders (Phidippus audax), crab spiders (Misumenops spp.), winter spiders (Chiracanthium inclusum), and striped lynx spider (Oxyopes salticus) (Johnson et al.,
1986). Supportive evidence for the selection of these taxa include data based
on observational studies (Whitcomb, 1967; Whitcomb and Bell, 1964; Wilson
t
Natural Control of Arthropod Pests
165
and Gutierrez, 1980, Wilson et al., 1980), radiolabeling studies (McDaniel
and Sterling, 1979, 1982; McDaniel et al., 198l), and cage studies (Lopez et
al., 1976). Other predators that may qualify as key predators in certain areas
include damsel bugs (Nabis spp.), Collops spp., assassin bugs (Zelus and
Sinea spp.), lady beetles (Hippodamia and Coleomegilla spp.), star-bellied
orb weavers (Acanthepeira stellafa), grey dotted spiders (Aysha gracilis),
long jawed orb weavers ( Tetragnatha laboriosa), and ridgefaced crab spiders
(Misumenoides formosipes) (Sterling, 1983). The age structure of predator
and prey may be critical in determining which of the predators above can
be classified as a key predator. Stimac and O'Neil (1985) have suggested
von Forester equations for dealing with age changes in time. Most predators
of Heliothis eggs and small larvae are small predators such as ants, minute
pirate bugs, big-eyed bugs, cotton fleahoppers, and immature spiders such
as black and white jumping spiders and winter spiders. Larger predators or
social hunters are needed to overcome the defenses of Heliothis larvae. Adult
leafhopper assassin bugs, fire ants, large winter spiders, celer crab spiders,
grey dotted spiders, black and white jumping spiders, and some earwig species can successfully attack and kill full-grown larvae.
In studying Heliothis predation by four generalist predators, R. E. Jones
et al. (unpubl. data) found that each predator differed in its response to
temperature, prey availability, and prey density. Geocoris, for example,
appeared most sensitive to high temperatures, with peak activity occurring
at about 26°C. At first this may seem surprising, since big-eyed bugs can
usually be found on cotton plants during the heat of the day. Closer examination, however, revealed that many of the Geocoris have moved down
the plant or onto the ground during the hotter hours of the day. At the other
extreme, Chrysopa larvae appear very insensitive to high temperatures, with
their activity being highest at 39"C, the highest temperature for which data
were available. Although all four of these predators are generalists, and feed
upon practically any available prey not too large, fast, or equipped with
sufficient defenses, minute pirate bug and Chrysopa appear better able to
adjust to changes in numbers, types, and distribution of prey. These two
predators demonstrated a much greater ability to adjust their distribution to
match the distribution of the more readily available prey, while Collops and
Geocoris continued to spend the majority of their time feeding on the bottom
surface of leaves, even when Heliothis eggs were distributed equally on both
surfaces. Each of these predators differ, however in their vertical and structural distribution (Wilson and Gutierrez, 1980) and in their seasonality, and
were differentially affected by the above-mentioned factors. As a result, the
conclusion of the results from these and related studies is that the predator
complex is more effective considering the season as a whole than even the
most voracious of the species could be if it were acting alone.
Inaction levels suggested to control Heliothis species include those of
McDaniel and Sterling (1982), who proposed that a ratio of one key egg
predator to one Heliothis egg was sufficient to control the pest. Hartstack
166
Biological Control of Pest Populations
Table 7.3 Grouping and Efficacy of the Guild of Predators Known to Prey on the
Cotton Fleahopper
Efficiency Index
Species or Group
Striped lynx spider (Oxyopes salticus)
Jumping spiders (Salticidae)
Crab spiders (Thomisidae)
Green lynx (Peucetia viridans)
Star-bellied orb weaver (Acanthepeira stellafa)
Spotted lady beetle (Coleomegilla maculata)
Big-eyed bug (Geocoris punctipes)
(OEi)
1 .o
1 .o
1.o
0.7
0.7
0.3
0.3
et al. (1975) suggested a ratio of one effective natural predator per two Heliothis eggs. Other inaction levels have been proposed by Herrera Aranguena
(1965), who concluded that if 15 to 20% of cotton terminals are infested with
Rhinacloa spp., the rate of predation on Heliothis larvae should be approximately 80 to 100%. In Arkansas, farmers were advised to depend on natural
enemies if “beneficials” were present at 20 or more per 56-feet row of cotton
(Barnes et al., 1977). Fye (1979) suggested that 35,000 to 50,000 predators
per acre were sufficient to remove Heliothis daily. All of these estimates
are crude. As new evidence becomes available concerning the identification
of the “key predators,” predator-prey age-structure relationships, and
many other factors, the prediction of natural enemy efficiency should become sufficiently precise for use in pest management programs.
Cotton Fleahopper Several generalist predators have been observed to
prey on cotton fleahoppers. Certain species of spiders have been reported
preying on fleahoppers (Dean et al. 1987; Reinhard, 1926; Whitcomb and
Bell, 1964), and rates of parasitism up to 25% have been recorded (Ewing
and Crawford, 1939). Mussett et al. (1979) obtained a correlation (r = 0.62)
between the abundance of a complex of predators and the abundance of
cotton fleahoppers, indicating that fleahoppers explain about 38% of the
variation in predator abundance. These data suggest that fleahoppers are an
attractive source of energy for some predaceous arthropods.
To predict the impact of a guild of predators on the cotton fleahopper,
the guild is divided into seven groups and weights (OEi) are given to each
group according to efficiency (Table 7.3) (Hartstack and Sterling, 1986,
1988). Oxyopes salticus is assumed to be the most efficient predator of the
cotton fleahopper, so it is weighted with an efficiency index of 1. Other
predators are compared in efficiency to Oxyopes and their intraspecificgroup efficiency is weighted to values of 1 or less Oxyopes equivalents (OEi).
The total Oxyopes equivalents per unit area (OE,) is estimated by Eq. (7.1),
where Niis the number of individuals of species group i per unit (e.g., per
,
,
Natural Control of Arthropod Pests
167
hectare) area and OEi is the intraspecific-group weighted efficiency of individuals of species group i.
P
=
1 - exp [-0.6930E,/(OEsoS)]
(7.2)
The percent daily mortality of fleahoppers (P) is estimated with Eq. (7.2),
where -0.693 is a correction factor to adjust the exponential curve at p =
0.5, represents the OEs needed to kill 50% of the fleahoppers, and S is the
searching area (ranging from 1 to 7, depending on plant size).
Lygus Species Lygus spp. is another example of a “pest” that also functions as an entomophage. Wheeler (1976) has reviewed observations on the
predacious tendencies of lygus bugs which feed on soft-bodied arthropods.
Predation on the eggs of the beet armyworm (Spodoptera exigua) in California (Eveleens et al., 1973) by Lygus hesperus suggests that members of
this genus may also feed on the eggs of other pests, such as Heliothis spp.
and the pink bollworm. Reports of Lygus as important natural enemies of
crop pests have all involved egg predation (Wheeler, 1976). The impact of
this predation in cotton fields is not yet clear.
Lygus are generally conceived to be of importance as a pest more than
as a predator of other pests. Thus the natural enemies of this genus have
been evaluated. The natural predator complex of cotton fields in southern
California provided 53 to 76% control of L. hesperus in the egg and nymphal
stages (Leigh and Gonzalez, 1976). Geocoris pallens was a very effective
predator, while Nabis americoferus was effective in sleeve cages but not in
larger cages. Early stages of Nabis alternutus were able to prey successfully
on the first three instars of L. hesperus, while large N . alternatus nymphs
were able to attack and kill all Lygus instars (Perkins and Watson, 1972).
Chrysopa carnea was ineffective against L. hesperus.
The mymarid Anaphes ovijentatus and the braconid Euphoriana uniformis
are the dominant parasites in California (Clancy and Pierce, 1966). In alfalfa
fields the average rate of parasitization was 46.6% over 14 counties in California. However, A. ovijentatus may be injurious as well as beneficial since
they also parasitize the eggs of Nabis americoferus. This suggests the need
for great caution in importing parasites of mirid pests that may also parasitize
native natural enemies.
PinkBollworm The pink bollworm (Pectinophora gossypiella),is exposed
to predators only during the egg stage, part of the first larval stage, the laststage larvae, and as an adult. Orphanides et al. (1971) reported one neuropteran, one dermapteron, five Hemiptera, four Coleoptera, and nine spiders feeding on the pink bollworm in southern California. All except spiders
fed on eggs, while Orius tristicolor and Geocoris punctipes preferred first-
I
I
168
Biological Control of Pest Populations
stage larvae over eggs. Only larger predators and spiders were able to overcome and consume larger larvae. Based on laboratory studies, the following
egg predators, arrayed in order of effectiveness, were listed: second-stage
larvae of Chrysopa carnea, adults of Collops marginellus, Geocoris punctipes, adult Notoxus calcaratus, Nabis americoferus, and 0. tristicolor. In
field cage studies, Irwin et al. (1974) concluded that N . calcaratus and Spanagonicus albofasciatus adults were ineffective predators of pink bollworm
eggs. The most promising predators were N . americoferus and G . pallens,
which reach natural field densities of one and three per plant, respectively.
However, C. carnea, although an efficient predator rarely reached field densities above one per plant. Henneberry and Clayton (1985) added Collops
vittatus and Hippodamia convergens to the list. This guild of predators is
capable of removing more than 90% of pink bollworm eggs placed artificially
on plants in the field (Henneberry and Clayton, 1982).
Unfortunately, with the current “scorched earth” insecticide control
strategy used in insect management over a large percentage of the southwestern cotton regions, predator-induced pink bollworm mortality is of little
more than academic interest. The above-mentioned generalist predators in
such areas are not able to survive in sufficient numbers through the gauntlet
of insecticide sprays to enable them to inflict sufficient mortality to prevent
economic loss.
Spider Mites Three spider mite species are responsible for the majority
of mite damage to cotton in the United States. Strawberry spider mite, Tetranychus turkestani, twospotted spider mite, T. urticae, and Pacific spider
mite, T. pacificus, each predominate at different times of the season; however, any one or all three can be found throughout the crop’s growth and
development. Although primarily a pest of more arid regions of California’s
San Joaquin Valley, the relatively recent trend to an increased use of synthetic pyrethroids has exacerbated the severity and importance of spider
mites not only in California but over much of the world. Spider mites, unlike
most other cotton pests, have an ability to literally explode in numbers.
Were physical and biotic mortality factors not acting, a single-mated female
emerging from the soil or blowing into a 40-ha field early in the season could
result in sufficient numbers of mites to cause economic yield loss (L. T.
Wilson, unpubl. data). Normally, however, a complex of generalist predators
is able to contain spider mite densities below economically damaging levels.
Our understanding of the factors primarily responsible for mite abundance
was until recently, extremely limited. Gonzalez et al. (1982) reported that
big-eyed bug and minute pirate bug abundance were both very closely associated with mite abundance, However, neither of these predators appear
to reach densities sufficiently high early in the season to prevent spider mites
from rapidly reaching economically damaging levels. Gonzalez et al. (1982)
and Gonzalez and Wilson (1982) also reported the immature stages of the
western flower thrips, Frankliniella occidentalis, “actively feeding on Te-
Natural Control of Arthropod Pests
169
PHYSIOLOGICAL TIME (DEGREE DAYS > 12°C)
Figure 7.4 Seasonal abundance of western flower thrips in San Joaquin Valley cotton. L. T.
Wilson and D. Gonzalez (unpubl. data).
tranychus eggs, wherever the latter was congregated.” In studies conducted
from 1978 through 1984, Frankliniella was consistently the most abundant
arthropod found in the cotton, with its greatest abundance often coinciding
with the presquaring and early squaring periods of crop growth. This period
of colonization is particularly relevant in that none of the other generalist
or opportunistic predators are yet in abundance. D. Gonzalez (unpubl. data)
and Trichilo (1986) found further that flower thrips are an extremely voracious mite predator, with third instar nymphs able to damage over 70 mite
eggs over a 24-hour period under laboratory conditions.
High thrips densities (Fig. 7.4) combined with a high feeding potential
results in this species being unequaled in its ability to suppress early- and
midseason mite populations. Large-scale predator suppression experiments
conducted in California from 1981 to 1984 demonstrate that the use of a
broad-spectrum insecticide reduces the abundance of thrips and other predators and inevitably resulted in the initiation of nearly exponential mite population growth about 2 to 3 weeks hence (D. Gonzalez and L. T. Wilson,
unpubl. data). This set of experiments has provided useful information for
developing economic thresholds for spider mites on cotton (Ellington et al.,
1984; Wilson et al., 1983; Wilson, 1986), but equally important, they have
enabled the control potential of natural enemies, particularly thrips, to be
quantified, One of the most difficult aspects of pest management is predicting
170
Biological Control of Pest Populations
I.o
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1981 Cotton, Shafter
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PHYSIOLOGICAL TIME OD>12OC
(from planting)
Figure 7.5 Several patterns of spider mite infestation in San Joaquin Valley cotton. L. T. Wilson
and D. Gonzalez (unpubl. data)
whether a pest species will cause economic loss in the future, Heliothis spp.
or Lygus, for example, are both highly mobile, have a wide host range, and
within an individual field do not necessarily have an easily forecasted population pattern. Spider mites, on the other hand, have a monotonically increasing, then decreasing population pattern (Fig. 7 . 3 , lending itself to accurate prediction of future spider mite abundance (see Chapter 5, Fig. 5.12).
Wilson et al. (1985) reported that by using the early season rate of spider
mite increase they were able to predict with a high degree of accuracy up
to 5 weeks in advance when an economic infestation would develop. This
relatively simple regression procedure enables the combined impact of all
mortality factors to be evaluated without the complexity inherent in predator
efficacy weightings as necessary for evaluating the impact of generalist predators on some of the pests discussed above. If the rate of spider mite population increase exceeds a damage trajectory (Wilson, 1986), this implies
that the mortality agents are not sufficient and that economic loss will probably result at some future predicted date unless appropriate management
actions are initiated (Fig. 7.5).
Other Pests Observations of the natural enemies of pests such as cotton
aphids (Aphis gossypii), cotton leafworm (Alabama argillacea), and thrips
have been reported by Whitcomb and Bell (1964). Empirical evidence of the
impact of natural enemies on some secondary pests of cotton include the
impact of Telenomus mesillae and Collops marginellus to a stink bug. These
Natural Control of Plant Pathogens
171
natural enemies contributed an average of 61.4% mortality to the pentatomid
Euschistus impictiventris in Arizona cotton fields (Clancy, 1946). Life table
studies by Ehler et al. (1973) and Eveleens et al. (1973) suggested that several
of the same species of predators of Heliothis inflict major mortality on the
cabbage looper (Trichoplusia ni) and the beet armyworm (Spodoptera exigua). These predators include 0. tristicolor, G . pallens, N . americoferus,
and C. carnea. Predation rates on the cotton leafworm after a 48-hour exposure to the native predator guild was 88.7 and 88.4% for eggs and small
larvae, respectively (Gravena and Sterling, 1983). The predator guild of the
cotton leafworm was similar to the Heliothis guild and other lepidopterous
inhabitants of cotton agroecosystems. However, spiders were the dominant
predators of cotton leafworm larvae, whereas the above-mentioned Hemiptera were dominant predators of eggs.
Arthropod Control with Microbials
Pests of cotton are attacked by several naturally occurring microbials, including bacteria, protozoa, fungi, and rickettsiae (Falcon, 1971). Although
these microbials probably play a role in pest control, their density is not
generally monitored to assist in making pest management decisions. However, there is some dependence on the cabbage looper virus in pest management programs. Generally, loopers are controlled by this virus before
economic loss occurs (National Apademy of Sciences, 1975).
Microbials such as Bacillus thuringiensis and the nuclear polyhedrosis
virus, applied to the field as insecticides, have been used in the management
of Heliothis species in many areas of the world. The major advantage of
using microbial pathogens to control pests is that they inflict little or no harm
to other natural enemies. But their impact has generally been sufficiently
sporadic (Bell, 1981) that interest in their use seems to be waning. Emphasis
in the past has been placed on efforts to increase the effectiveness of arthropod pathogens by developing or identifying new, more virulent strains
of pathogens; improving spray formulations; and developing new methods
of applying or disseminating pathogens (Bell, 1983). None of these efforts
has met with notable success. One method of using microbials that seems
to have been largely overlooked is to find ways to monitor natural populations of pathogens as a management tool for predicting their impact on
arthropod pest population.
NATURAL CONTROL OF PLANT PATHOGENS
Since ancient times, man has practiced biological control of plant pathogens
through cultural practices such as the use of legumes in crop rotation, clean
tillage, and the use of organic manurial amendments. These practices provided for the biological destruction and/or suppression of disease organisms.
172
Biological Control of Pest Populations
Biological control aimed directly at the pathogen or mediated through adjustments in the host offers unlimited opportunities to reduce losses caused
by biotic and abiotic stresses. As in the case of arthropods, biological control
of plant pathogens should be regarded as one part of the total integrated pest
and crop management system. Its relative importance can be expected to
vary with different diseases, dominant in some instances where other measures have failed, but of minor importance where other measures provide
inexpensive, effective control.
Biological control of plant pathogens seeks a solution in terms of restoring
and maintaining the biological balance within the ecosystem and must be
considered part of modern agriculture. Biological control offers a powerful
means to improve the health and hence the productivity of plants by suppression or destruction of pathogen inoculum, protection of plants against infection, or increasing the ability of plants to resist pathogens.
Concepts and Mechanisms
The mechanisms of biological control of plant pathogens have been grouped
into three general categories: (1) reduction of inoculum by microorganisms
antagonistic to the target pathogen, (2) protection of host plant surfaces by
antagonists, and (3) management of physiological incompatibility between
host and pathogen obtained by genetic change in the host or by inoculation
with an avirulent or nonpathogenic microorganism (Baker, 1968; Baker and
Cook, 1974; and Cook and Baker, 1983).
Antagonists of plant pathogens may be introduced or resident (Garrett,
1965). Introduced antagonists are prepared products applied to the soil, seed,
or plant to control a pathogen. Resident antagonists are part of the natural
microbiota in soil or on roots, leaves, fruit, or other plant parts.
The equilibria of microorganisms in the agroecosystem are established as
a result of antagonistic processes: competition, antibiosis (including fungistasis), exploitation, and hyperparasitism. All of these types of antagonism
occur commonly, especially in soil, and all can influence the activity of plant
pathogenic microorganisms. For example, a soilborne pathogenic fungus
may be subject to fungistasis, antibiosis (which can inhibit vegetative
growth), competition from other organisms for colonizeable organic matter
in soil upon which the fungus is dependent for an energy source to reproduce
itself, and parasitism by other microorganisms upon vegetative and survival
structures (hyperparasitism) (Papavizas and Lumsden, 1980). Hyperparasitism refers to the control of pathogenic microorganisms with other microorganisms or viruses which parasitize or antagonize the pathogen. The best
known cases of hyperparasitism include the bacteriophages, mycoparasites,
and nematophagous fungi.
The protection of plant surfaces by antagonists and the management of
host pathogen incompatibility have emerged as necessary strategies because
plant pathogens commonly exist in close association with their hosts, and
1
Natural Control of Plant Pathogens
’
.
173
many complete most or all of their life cycle inside the host plant. Obviously,
the host has a biological system of its own which must be intimately involved
in the biological control of these pathogens.
Antibiosis is the most widely recognized mechanism that may cause inactivation or destruction of soilborne plant pathogen propagules preventing
germination. Antibiosis is used in plant pathology to describe the chemical
inhibition of one microorganism by another, which is more parallel to allelopathy, whereas usage in entomology describes a mechanism of host plant
resistance to a pest.
The specific form of antagonism may be mediated by specific toxic metabolites of microbial origin, by soil fungitoxins, and by lytic agents (Jackson,
1965). Antibiosis in soil can also result from elevated fungistasis or liberated
inhibitory volatiles. If fungal propagules are not inactivated by antagonism
or reduced in numbers below economic threshold levels in the dormant state
or during germination, biological control may still be possible by preventing
certain processes or functions. These include lysis and mycoparasitism of
mycelia, suppression of germling growth and sporulation, hypovirulence and
mycoviruses, and cross protection (Garrett, 1965; Baker, 1968; Baker and
Cook, 1974; Papavizas and Lumsden, 1980; Cook and Baker, 1983). Viruses
or virus-like agents specific for the pathogen may reduce virulence, aggressiveness, or survival ability of the pathogen (Ghabrial, 1980).
Bird (1982) hypothesized that microorganisms (bacteria, fungi, and actinomycetes) which are natural colonizers of the plant tissues and root surfaces (symbiotic organisms) have a major role in resistance to diseases and
insects, and are under the genetic control of the host. Components of seed
and root exudates of Tamcot multi-adversity resistance (MAR) cotton cultivars can selectively influence rhizosphere-rhizoplane population levels of
bacteria and actinomycetes (Batson, 1972; Tsai and Bird, 1975; Bush, 1980).
Bird et al. (1979) and El-Zik et al. (1985) have shown that the concentrations of symbiotic organisms associated with plant parts (leaves, terminals,
and squares) were much higher in MAR than in non-MAR cottons (see Chapter 8). The predominant symbionts were Bacillus spp., which were designated smooth white (SW) and rough white (RW), based on their colony
characteristics when grown on Allen’s soil extract agar. Recently, the SW
bacterium was identified as Bacillus megaterium and the RW as B. cereus
(Howell et al., 1987). Evidence that symbiotic organisms isolated from Tamcot CAMD-E influence the response of the host to the bacterial blight pathogen, Xanthomonas campestris pv malvacearum (Bird et al., 1979; El-Zik
et al., 1983), seedling pathogens and Phymatotrichum omnivorum (Bird et
al., 1979, 1980), and boll weevil (Benedict et al., 1979) has been reported.
Baker (1968), Baker and Cook (1974), Papavizas and Lumsden (1980),
Cook and Baker (1983), and Baker (1985) have provided extensive reviews
on biological control and its principles and mechanisms. The potential for
biological control of plant diseases on the phylloplane has recently been
l
174
Biological Control of Pest Populations
reviewed by Blackeman and Fokkema (1982) and Windels and Lindow
(1 985).
Approaches to Biological Control of Cotton Pathogens
One may consider biological control of cotton pathogens by reducing inoculum density equivalent to biological control of insects: namely, the re- ,
.
duction of the insect population to an economically acceptable threshold
level. A number of actinomycetes, bacteria, and fungi have been isolated
from soil and plant surfaces, and some have shown potential as biological
control agents. Under laboratory and controlled growth conditions they perform quite well; however, a large number fail to control disease consistently
under field conditions.
Recent research has focused on utilizing microbes isolated from the cotton
rhizosphere and rhizoplane as biological agents to control seed-seedling
pathogens. Hagedorn et al. (1985) identified 17 different genera of bacteria
from the cotton rhizosphere and rhizoplane. They tested several isolates
from these genera on field-grown cotton and obtained biological control
against the seed-seedling pathogens Pythium uftimum and Rhizoctonia
solani.
Gfiocfadium spp. are resident antagonists in soils, reducing populations
of selected fungi. Howell (1982) found that G. virens parasitized R. sofani
and inhibited P. uftimum by antibiosis. Damping-off of cotton seedlings was
reduced when the antagonist was placed in soil with the seed.
Howell and Stipanovic (1979, 1980) obtained improved emergence of cotton seedlings by treating the seed with strains of Pseudomonas jluorescens
isolated originally from the rhizosphere of cotton seedlings. Treatment of
cotton seed with strain Pf5 of P. fluorescens improved seedling survival from
30 to 79% and 28 to 71% in soil infested with R. sofani and P. uftimum,
respectively. Ideally, antagonists should be effective against several pathogens or strains of a pathogen; however, it has been shown that antagonists
can have a high degree of specificity. Howell and Stipanovic (1979, 1980)
isolated two chlorinated phenyl pyrrole antibiotics from P. jluorescens. The
antibiotic pyrrolnitrin inhibited R . sofani in vitro but was ineffective against
P. ultimum, and the antibiotic pyoluteorin was extremely inhibitory to P.
uftimum but not to R . sofani. Treatment of cotton seed with the antibiotics
alone gave improved emergence and decreased damping-off in soil infested
with R. solani and P. uftimum, respectively. Pyrrolnitrin was also effective
against Thefaviopsis basicofa, Verticillium dahfiae,and Alternaria spp. Elad
et al. (1982) showed that coating cotton seed with Trichoderma hamatum
or T. harzianum decreased damping-off of cotton seedlings in field tests.
Yin et al. (1957, 1965) in China selected a Streptomyces sp. from among
4000 isolates of actinomycetes from roots of cotton and alfalfa on the basis
of its in vitro antibiosis to R . sofani and V . afbo utrum. This culture, strain
\
Natural Control of Plant Pathogens
175
5406, has been used on 15 million acres of cotton over a 30 year period,
giving increased crop growth (Cook and Baker, 1983).
In recent years, considerable attention has been devoted to mycorrhizal
fungi, which have been shown to provide effective protection of feeder roots
against soilborne pathogens such as Phytophthora, Pythium, and Fusarium.
In addition, mycorrhizal fungi increase the uptake of phosphorus and other
nutrients of plants, and generally improve plant growth and health.
Under controlled conditions, Thelaviopsis basicola caused less stunting
of cotton and tomato when endomycorrhizae were present in their roots as
compared with the same host with roots lacking mycorrhizae. Roncadori
and Hussey (1980) have shown that VA-mycorrhizae Gigaspora margarita
and Glomus etunicatus are both excellent symbionts on cotton, and in fumigated low-phosphorus soil may improve early plant growth by as much
as 600%. When each mycorrhizal fungus was challenged in greenhouse studies with root-knot nematode, stunting caused by Meloidogyne incognita was
completely nullified and there was no effect on root or shoot biomass. Although both G. margarita and G. etunicatus nullified stunting caused by M .
incognita, their effects on nematode reproduction were different. Only mycorrhizae formed with G. etunicatus significantly reduced the egg populations of M. incognita. Smith et al. (1986) found that G. intraradices and G.
margarita can increase host tolerance to the root-knot nematode under field
conditions and reduce the severity of yield loss.
Monoculture and suppressive soils have been reported to cause natural
disease reduction. Monoculture decline occurs when continuous cropping
with a susceptible crop results in a decrease of disease incidence (Shipton,
1977), and soil suppressiveness develops as a natural reduction in disease
incidence (Baker and Cook, 1974; Cook and Baker, 1983).
Many groups of organisms have been cited as candidates for the biotic
suppressive factor in disease suppressive soil (Hornby, 1983; Papavizas and
Lumsden, 1980; Cook and Baker, 1983). King et al. (1934) first showed that
heavy application of organic matter controlled Phymatotrichum root rot of
cotton. This was confirmed by Clark (1942), who related the rate of breakdown of organic matter to the rate of death and decomposition of sclerotia
of the pathogen.
Many species of soil microarthropods have been reported to be predominantly mycophagous and may have a role in biological control of soil microorganisms. Curl (1979) and Wiggins and Curl (1979) found that two species
of collembola (Proisotoma minuta and Onychiurus encarpatus) feed on
hypae of R . solani, possibly reducing inoculum density of the pathogen in
the root zone. In addition, collembola can transmit and inoculate the cotton
seedling root zone with antagonistic and pathogenic sporulating fungi. Curl
(1982) reported that effective biological control of pre- and postemergence
damping-off of cotton seedlings was obtained by adding collembola to the
soil in populations of 909 lb/acre under experimental conditions.
Control of nematode pests by biological agents is a practice which has
176
Biological Control of Pest Populations
I
not been particularly successful to date, although a wide range of predators
and parasites attack nematodes. Duddington and Wyborn (1972) have reported about 50 known species of predacious fungi that either capture or
kill nematodes in the soil. Van Gundy (1972) listed, in addition to the 50
known species of fungi, two protozoans and numerous other small invertebrates in the soil that had been reported to destroy or to feed on nematodes.
Mankau (1980, 1981) reviewed biological and microbial control of nematode pests. The bacterium Bacillus penetrans has shown promise as a
control agent, and has a life cycle remarkably adapted to parasitism of rootknot nematodes (Mankau, 1980, 1981). Recent discovery of several fungal
parasites of nematode eggs and cysts has expanded interest in biological
agents (Mankau, 1980, 1981).
Current Status of Biological Control of Plant Pathogens
There are few biocontrol agents of plant pathogens presently employed in
agriculture despite long-term research efforts in many public laboratories
and the more recent increase in industrial research efforts. A major limitation
on the current use of biological control agents has been the inconsistent
results achieved when applied under field conditions. Following the initial
discovery and testing of biocontrol agents, much work needs to be done
concerning the various aspects of industrial microbiological application. The
main problem in application is in managing the host, environmental conditions, and the agent itself so that the activity of the biocontrol agent is
enhanced.
Antagonists of plant pathogens are largely passive and relatively nonmobile, and make accidental contact with pathogens. Therefore, biological
control agents of plant pathogens must be applied directly to the locality
where infection will occur. Antagonists must be in high concentrations at
the infection sites, such as the leaf surface, to control a leaf-infecting pathogen, or on seeds or roots to control soil pathogens. A major difference
between controlling arthropods and plant pathogens with biocontrol agents
lies in the mechanisms that affect their populations. Biological control of
plant pathogens has been effected principally by competition and antibiosis,
and sometimes hyperparasitism, whereas biological control of insects is
mainly by predation, parasitism, and disease. Many effective cultural methods currently in use promote and enhance biological control of plant
pathogens.
The challenge has been to identify the biological agents and gain a thorough understanding of mechanisms and factors, both biotic and abiotic, that
affect their behavior. More research is needed on the mechanisms involved
in biological control, their interaction with biotic and abiotic agents, and the
influence of environment. At present, the problems of application, stability,
cost, effective duration of the biological control agent, and other aspects
have not been perfected sufficiently to allow commercialization.
I
Natural Control of Weeds
177
NATURALCONTROLOFWEEDS
The principles and procedures for biological control of weeds are well established (Huffaker, 1959; Andres, 1977; Templeton et al., 1979; Charudattan
and Walker, 1982; Charudattan, 1985; Templeton, 1982). Several successful
examples of biological agents for weed control, including phytophagous insects and plant pathogens, have been reported; however, many biological
control agents are usually highly specific, resulting in a very narrow spectrum of weeds controlled by a single pest. Although bacterial and viral plant
pathogens have been examined, all the microbial weed control agents that
are in use or under development in North America are fungal pathogens.
There has been limited success using insects and plant pathogens to control major weeds in cotton. Augmentation of biocontrol agents may be used
to overcome some of the limitations. In Mississippi, the native moth Bactra
verutana attacks purple nutsedge, Cyperus rotundus, but it is ineffective
since too few moths overwinter. By the time the moth population has increased, the nutsedge is so vigorous that larval feeding cannot control new
shoots. Frick and Chandler (1978) reported that early season inundative
release of mass-reared B. verutana larvae and adults in cotton fields allowed
larvae to suppress nutsedge, resulting in seed cotton yields equal to those
in herbicide-treated or nutsedge-free fields.
Recent advances in biological control of weeds have shown that plant
pathogens can control weeds within crops when properly employed. Walker
(1980) reported that levels of spurred anoda, Anoda cristata, were reduced
75% with a 100% leaf infection when the fungus Alternaria macrospora was
applied as a single foliar spray to seedlings in the two- to three-leaf stage.
Colletotrichum malvarum causes an anthracnose of prickly sida, Sida
spinosa. Control of prickly sida with the mycoherbicide, C. malvarum, in
the field has been erratic and dependent on environmental conditions at the
time of inoculum application. Maximum control (90 to 95%) was achieved
when inoculum was applied while cool (24"C), moist conditions prevailed
for several days following inoculation (TeBeest, 1981). In field tests, one
application of a spore suspension (2 x IO6 spores/mL) of C. malvarum in
September at the rate of 378 L/hectare reduced the density of prickly sida
by 98%. However, results of identical tests conducted in July did not result
in control of prickly sida at any inoculum concentration tested (TeBeest,
1981). The major constraints to the effective use of plant pathogens as biocontrol agents are environmental conditions, such as temperature and duration of free moisture, required for infection and disease development; and
the necessity for multiple inoculum applications to control the repeated
emergence of new weed seedlings. On the positive side, mycoherbicides can
easily be applied using the same techniques and equipment for herbicides.
Orr (1981) found that silverleaf nightshade is naturally parasitized by the
nematode Nothanguina phyllobia. The nematode injures the weed by reducing its growth and development, vigor, and seed production. Nematode-
178
Biological Control of Pest Populations
infecting larvae overwinter in the soil or in infested plant tissues, and attack
silverleaf nightshade plants at emergence or any time during the growing
season when environmental conditions are favorable. After four years, over
80% control of silverleaf nightshade was achieved using N . phyllobiu in two
field tests (On,1981).
Geese have been used successfully for many years and have given economic control to grasses in cotton. Geese will feed on johnsongrass, burmudagrass, nutsedge, and annual grasses; however, they do not control
cocklebur or pigweeds. Three to five 6-week-old geese per acre are generally
effective (Miller et al., 1977). However, several management problems must
be considered when geese are used. These include constant availability of
clean drinking water, supplemental feeding, providing shade, protection
from predators, and fencing.
The use of insects and plant pathogens in biological control is an exciting
and rapidly expanding area in weed science and has potential for broad
application. Biological weed control agents may be incorporated and integrated with other pest control strategies and crop management systems.
TOWARD CLASSICAL BIOLOGICAL CONTROL
The introduction of exotic agents for the biological control of arthropod and
weed pest species in cotton may have little or no chance of success if repeated applications of broad-spectrum insecticides continue to be used in
the cotton agroecosystem. Few predators of insects, pests, or plants can
survive and maintain levels necessary for control of insect or weed pests if
exposed to repeated insecticide sprays. Thus a prerequisite to the use of
classical biological control may be to eliminate broad-spectrum pesticides
from the ecosystem; or as a minimum, severely curtail the number of sprays
applied during a season. The instant elimination of all insecticides from cotton production is not likely to be economically feasible. Some cotton regions,
such as California’s lower desert valleys, are essentially addicted to chemical
pesticides (van den Bosch, 1978). Were insecticide usage to be instantly
stopped in such areas, the resultant damage would probably be catastrophic.
Farmers in highly disturbed production systems are dependent on chemicals
in order to obtain high yields. Thus if a community of farmers should choose
to change their chemical-intensive production approach and instead to control pests with a judicious combination of pesticides and natural biological
control, a period of chemical “withdrawal” may be necessary to evolve into
a chemically rational system. Under such a system insecticide use must be
integrated in a way that will minimize or eliminate the impact on the native
natural enemies.
Augmentation of Natural Enemies
Theoretically, the augmentation of natural enemies to control cotton pests,
particularly the Heliothis spp., should provide a method that would not de-
\
Natural Control of Weeds
177
NATURAL CONTROL OF WEEDS
The principles and procedures for biological control of weeds are well established (Huffaker, 1959; Andres, 1977; Templeton et al., 1979; Charudattan
and Walker, 1982; Charudattan, 1985; Templeton, 1982). Several successful
examples of biological agents for weed control, including phytophagous insects and plant pathogens, have been reported; however, many biological
control agents are usually highly specific, resulting in a very narrow spectrum of weeds controlled by a single pest. Although bacterial and viral plant
pathogens have been examined, all the microbial weed control agents that
are in use or under development in North America are fungal pathogens.
There has been limited success using insects and plant pathogens to control major weeds in cotton. Augmentation of biocontrol agents may be used
to overcome some of the limitations. In Mississippi, the native moth Bactra
verutana attacks purple nutsedge, Cyperus rotundus, but it is ineffective
since too few moths overwinter. By the time the moth population has increased, the nutsedge is so vigorous that larval feeding cannot control new
shoots. Frick and Chandler (1978) reported that early season inundative
release of mass-reared B . verutana larvae and adults in cotton fields allowed
larvae to suppress nutsedge, resulting in seed cotton yields equal to those
in herbicide-treated or nutsedge-free fields.
Recent advances in biological control of weeds have shown that plant
pathogens can control weeds within crops when properly employed. Walker
(1980) reported that levels of spurred anoda, Anoda cristata, were reduced
75% with a 100% leaf infection when the fungus Alternaria macrospora was
applied as a single foliar spray to seedlings in the two- to three-leaf stage.
Colletotrichum malvarum causes an anthracnose of prickly sida, Sida
spinosa. Control of prickly sida with the mycoherbicide, C. malvarum, in
the field has been erratic and dependent on environmental conditions at the
time of inoculum application. Maximum control (90 to 95%) was achieved
when inoculum was applied while cool (24"C), moist conditions prevailed
for several days following inoculation (TeBeest, 1981). In field tests, one
application of a spore suspension (2 x IO6 spores/mL) of C. malvarum in
September at the rate of 378 L/hectare reduced the density of prickly sida
by 98%. However, results of identical tests conducted in July did not result
in control of prickly sida at any inoculum concentration tested (TeBeest,
1981). The major constraints to the effective use of plant pathogens as biocontrol agents are environmental conditions, such as temperature and duration of free moisture, required for infection and disease development; and
the necessity for multiple inoculum applications to control the repeated
emergence of new weed seedlings. On the positive side, mycoherbicides can
easily be applied using the same techniques and equipment for herbicides.
Orr (1981) found that silverleaf nightshade is naturally parasitized by the
nematode Nothanguina phyllobia. The nematode injures the weed by reducing its growth and development, vigor, and seed production. Nematode-
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179
stroy natural enemies which regulate the pests and that could be used to
replace insecticides when resistance develops (Ridgway et al., 1973). AIthough technically feasible (Ridgway and Morrison, 1985), the economic
feasibility has seldom been demonstrated in the United States. King et al.
(1985) reviewed augmentation projects with 29 different species in reaching
this conclusion concerning economics. More specifically, they reported that
it is not feasible to manage Heliothis spp. in cotton by augmentative releases
of Trichogramma pretiosum, one of the most ambitious projects yet attempted in the United States (Stinner, 1977). Other reviews of augmentation
(Ridgway and Morrison, 1985; Ridgway and Vinson, 1976) indicate the feasibility of the augmentation approach in countries, such as in the Soviet
Union and China, where labor is considerably cheaper. Although several
parasites and predators can be purchased in the United States, federal and
state entomologists have generally not recommended their use in cotton.
Thus the augmentation approach to biological control of arthropod pests
of cotton is currently being used on a limited basis in the United States
but largely awaits more efficient natural enemies or cheaper production
methods.
Restoration Ecology
For a farmer to take advantage of nonchemical means of controlling cotton
insect pests, some cotton agroecosystems will require restoration. It is rather
simple for a farmer using a “natural control” strategy to change to a chemical
strategy. However, returning to a noninsecticidal strategy following heavy
use of insecticides may be more difficult. It may take as long as three years
for the natural enemy fauna to recover completely following multiple applications of broad-spectrum insecticides (Bartlett, 1964). Restoring the efficiency of the natural enemies may be virtually impossible in a community
where several neighbors are using an intensive insecticidal strategy.
Barring resistance to insecticides, it is generally possible to achieve high
yields and profits using an intensive insecticide program for pest control.
However, if for whatever reason the insecticides lose their effectiveness,
growers in some areas can switch to a cotton production system using minimal applications or no insecticides. A pertinent question is: How is it possible to rely on natural control or increase its effectiveness when needed
while minimizing the risk of crop loss? California and Texas growers often
rely on natural control almost exclusively; control measures are normally
required only during relatively brief periods of the growing season. To aid
them in their decision-making process, growers can take periodic samples
of pests and natural enemies in cotton fields to determine if sufficient natural
enemies are available to prevent unacceptable losses by the pests (Sterling,
1984). This tactic adds the additional cost of sampling to production costs,
so for sampling to be a feasible tactic, it should provide economic and ecological benefits that exceed the sampling costs. Under current integrated
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Biological Control of Pest Populations
pest management programs for cotton, lip service is given to the sampling
and use of natural enemies. But since few “inaction levels” are available
to assist the decision maker, most management decisions are based on the
abundance of pests with insufficient regard for the abundance of natural
enemies. On the other hand, the decision made by some farmers to grow
cotton without insecticides is probably also made “automatically” without
regard to the density of natural enemies or pests. This decision is also not
likely to be optimal and could probably benefit from better information on
the density of natural enemies and pests.
As the true role of natural enemies in the cotton agroecosystem is determined, and effective inaction levels are made available for key natural
enemies, management decisions should often be improved by counting the
natural enemies to predict their potential impact on the pest species. However, this tactic is likely to be unprofitable for those growers who choose
either end of the tactical spectrum. Few events in cotton fields can be predicted with a high level of reliability. However, one characteristic of cotton
fields and their associated fauna and flora that is highly predictable is that
there will be constant change. Plants grow or die, arthropods, plant pathogens, and weeds increase or decrease in numbers, and weather changes. No
two years are the same with regard to plant growth, pest population dynamics, or weather. Thus it is unlikely that automatic application of production
tactics will be optimal. To achieve optimal decisions, the availability of reliable information is critical. Thus sampling to obtain reliable information
concerning the density of natural enemies should add to the reliability of
pest management decisions (see Chapter 5).
Classical Biological Control
“No effective exotic natural enemy of the boll weevil has been imported
and permanently established in the US” (Cate, 1985). Of about 15 species
of entomophagous insects that have been imported and released against Heliothis spp., none have so far been successful (Johnson et al., 1986). The
same is essentially true for other key pests of cotton. For example, at least
nine parasite species have been introduced into the United States for control
of the pink bollworm, and none have become established (Clausen, 1978).
Although the potential exists for the classical introductions of foreign biological control agents into cotton for pest control, the risk of failure appears
to be fairly high, due largely to the durational instability of the cotton crop
and the use of broad-spectrum insecticides for pest control. Success rates
for introductions might be increased by restoring the ecosystem to reduce
or eliminate the insecticidal contamination in communities where releases
are made. According to Beirne (1979, the establishment rate of introduced
natural enemies into Canadian annual crops is 16%. Thus it would appear
superficially that a similar low probability of successful establishment is
possible in a cotton agroecosystem.
I
References
181
CONCLUSION
All cotton pests would cause greater damage to the crop if natural enemies
were absent. It is likely that cotton could not generally be grown profitably
without the impact of naturally occurring predators, parasites, and pathogens
(van den Bosch and Hagen, 1966). However, the full benefit of natural enemies is not being realized on millions of acres of cotton grown in the world
that are currently dependent on chemical pesticides for control. The wise
use of natural enemies could result in a reduced pesticide load on the environment and greater long-term economic benefit to the farmers.
The advantage of using natural enemies over complete reliance on chemicals is that native natural enemies voluntarily colonize cotton fields, they
are self-multiplying, they can be very effective, they do not pollute the ecosystem, and they cost the farmer nothing. To realize the advantage of using
natural enemies, there is an urgent need to identify the key natural enemies
for each pest and to establish inaction levels for use in pest management
decisions. This information, used together with reliable monitoring programs
and predictive computer models, should make it possible to determine when
not to intervene in the dynamics of pests and their natural enemies with no
or limited risk to the cotton farmer.
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