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PESTICIDE
RESISTANCE IN BENEFICIAL ORGANISMS
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Overview A review of natural enemy
resistance to pesticides by Tabashnik & Johnson (1999) considered that
beneficial species account for less than 3% of the 447 species of insects and
mites known to be resistant to one or more pesticides (Georghiou 1986).
Therefore, documented cases of resistant pest species outnumber those in
natural enemies by more than 30 to 1. Reasons for this disparity are due to
(1) biases in documentation, (2) differential preadaptation to pesticides and
(3) differences in population ecology. Tabashnik & Johnson emphasize that
the various hypotheses attempting to explain why reported cases of resistance
in pests greatly outnumber those in natural enemies are not mutually
exclusive. Combinations of factors may operate in a given case and the
relative importance of each factor may vary among species. Therefore, there
is no single explanation. Pesticide resistance is a
genetically based, statistically significant decrease in response of a
population to a pesticide. The measured response is usually acute mortality,
but changes in sub lethal or long-term responses are not excluded. Pesticide
resistance may be demonstrated by a decrease in mortality through time for a
given population, or by decreased mortality of a population relative to
conspecific populations. Unlike some definitions of resistance (Georghiou
1981), that of Tabashnik & Johnson (1999) does not specify the extent of
change in response to the pesticide nor does it imply the ability to survive
field applications of pesticide. Various hypotheses proposed to
explain the scarcity of documented cases of resistance in natural enemies are
not mutually exclusive. The relative importance of each factor may vary among
species and among pesticides; and several factors may act jointly in some
cases. Thus, there is no single general explanation. A review of available
evidence casts doubt on some hypotheses, supports others and indicates
potentially productive areas for research. Resistance is more likely to be
documented for pests than natural enemies, but the magnitude of this effect
is difficult to measure. Bioassays comparing interpopulation variation for
several pests and natural enemies from a given crop and region could help to
assess the influence of documentation bias. Natural enemies apparently do not lack the detoxification
enzyme systems found in pests and intrinsic levels of detoxification enzymes
are not consistently higher for pests than for natural enemies. For cases in
which pests do have higher levels of detoxification enzymes than natural
enemies, there is little evidence showing that this difference contributed to
faster evolution of resistance in the pest. Versions of a preadaptation hypothesis
based on intrinsic differences in detoxification ability appear unsound. The
overall differences in intrinsic pesticide tolerance between pests and
natural enemies are difficult to assess, but there are many cases in which
pests are more tolerant than natural enemies. Higher intrinsic tolerance in
pests could account in part for more documented cases of resistance in pests,
particularly if the criteria for resistance include the ability to survive
field applications of pesticides. Lack of genetic variation for pesticide
tolerance in natural enemies could also retard their evolution of resistance.
There is indirect evidence to suggest that differences in
population ecology are important in slowing resistance development in natural
enemies relative to pests. However, differences in genetic systems and
related factors are not apt to explain why pests evolve resistance more
readily than natural enemies. Food limitation due to reduction in host or
prey populations by pesticides is believed to be a major factor influencing
natural enemy populations. The
decimation of arthropod populations in insectiicide treated apple orchards is
known to be enormous (Please refer to Related Research ). If this is true
then there are some important implications for management. Natural enemies
that are provided abundant food in artificial selection programs should be
capable of evolving pesticide resistance (Hoy 1985, 1989). Also, intensive pesticide use may disrupt
biological control, even if the natural enemies are relatively tolerant
(either naturally or due to selection) (Tabashnik 1986). Therefore, in order
to maintain effective biological control, the use of selective pesticides
should be sparing and judicious.Following is a detailed review of some of
these considerations: Pest resistance to pesticides can cause control failures and
attract immediate attention. In contrast, natural enemy resistance to
pesticides does not obviously create problems and may go unnoticed.
Therefore, pesticide resistance is more likely to be documented in pests than
in natural enemies (Georghiou 1972, Croft & Brown 1975). It has been noted that if resistance in natural enemies
appears rare due to inadequate documentation, then systematic testing of
samples of natural enemies in heavily treated ecosystems should detect more
cases of resistance (Croft & Brown 1975). According to extensive surveys,
data available on pesticide impact on natural enemies more than doubled from
1970 to 1985 (Theiling & Croft 1988) and the number of natural enemy
species reported as resistant to one or more pesticides also doubled during
the same period (Georghiou 1972, 1986). The proportion of cases of resistance
accounted for by beneficial species nevertheless remained at about 3% in the
1970 and 1984 surveys. These data show that the cumulative effect of factors
contributing to more documented cases of resistance in pests than in natural
enemies has remained consistent through time. Cases of resistance were included in the previous mentioned
surveys only if it was due to field application of pesticides and was
sufficient to cause diminished mortality at field application rates
(Georghiou 1981, 1986). Cases of resistance in natural enemies due to field
and laboratory selection are reviewed elsewhere (Croft & Strickler 1983,
Croft 1989, Hoy 1989). Before 1979 Croft & Strickler (1983) document
cases of pesticide resistance among arthropod natural enemies. Phytoseiid mites received considerable attention in the period
after 1979, and had higher levels of resistance than other natural enemies. A
significant difference in susceptibility between at least one pair of
populations was reported in 77% of cases for phytoseiids. Maximum resistance
ratios for phytoseiids exceed 10 in 40% of cases. Field survival, as
indicated by a maximum LC50 greater than recommended application
rates, was reported in 6 of 12 cases. For non-phytoseiid natural enemies, 74%
of cases showed significant variation in susceptibility among conspecific
populations, but maximum resistance ratios exceeded 10 in only 11% of cases
and 35% of cases showed field survival. Five of six cases showing ability to survive field
concentrations of pesticide in non-phytoseiids was due to Chrysoperla carnea (Stephens). The ability
to survive field rates in these five cases represents natural tolerance
rather than resistance, because LC50's of the most susceptible
populations exceeded recommended field concentrations. In fact, four of the
five cases were due to tolerance to pyrethroids that were not registered for
field use when the bioassays were performed (Grafton-Cardwell & Hoy
1985). Excluding the cases due to tolerance in C. carnea,
field survival was reported in only one of 11 (9%) cases for non-phytoseiid
natural enemies (Aphidoletes
aphidimyza (Fondani) vs.
azinphosmethyl). Almost all studies of Hymenoptera have shown significant
variation in susceptibility among populations (92%), but high levels of
resistance were virtually absent. Only Comperiella
bifasciata Howard had a
resistance ratio greater than 10, and no Hymenoptera population had an LC50
greater than recommended field rates. The few cases reviewed here suggests
that significant variation in susceptibility to pesticides among conspecific
populations is common in natural enemies, but resistance conferring survival
at field application rates is rare in natural enemies other than phytoseiid
mites. Phytoseiids may evolve resistance readily because they have many
generations per season, they are exposed to pesticides in all life stages,
they have limited dispersal, and they subsist on plant materials when prey
density is low (Georghiou 1972, Croft & Brown 1975, Hoy 1985, Croft &
van de Baan 1988). Differential
Preadaptation Hypothesis The overall pattern shows that indeed pests evolve resistance
more readily than natural enemies, with several factors involved in slowing
development of resistance in natural enemies. Four hypotheses are (1) that
pests have better intrinsic detoxification capabilities than natural enemies
(Gordon 1961, Croft & Morse 1979, Croft & Strickler 1983), (2) pests
evolve resistance more readily because they have greater intrinsic tolerance
to pesticides than natural enemies, (3) pests have more genetic variation in
tolerance to pesticides than natural enemies (Georghiou 1972), and (4) the
fitness cost associated with resistance is lower for pests than natural
enemies. These explanations are related and not mutually exclusive. All
have two parts (1) there is some intrinsic (i.e., before pesticide exposure)
difference between pests and natural enemies in their response to pesticides
and (2) the intrinsic difference enables pests to develop resistance more
readily than natural enemies. Differences in
Detoxification Enzymes.--Croft & Strickler (1983) review different
detoxification enzymes. The idea is that herbivorous pest insects have
evolved enzymes to detoxify plant secondary compounds and are then better
preadapted to detoxify pesticides than are entomophagous natural enemies
which do not eat plants. In the broadest survey to date, Brattsten &
Metcalf (1970) used the synergistic ratio of carbaryl with piperonyl butoxide
to compare levels of mixed function oxidase (MFO) detoxification enzymes in
53 insect species from 8 orders. Piperonyl butoxide inhibits MFO enzymes that
detoxify carbaryl. Thus, the ratio of the LD50 or LC50
of carbaryl alone to that of carbaryl plus piperonyl butoxide (synergistic
ratio) is an indicator of MFO activity. Brattsten & Metcalf (1970) found that a few of the
phytophagous species had extraordinarily high synergistic ratios (e.g., Pogonomyrmex barbatus (F.Smith)), the red
harvester ant ratio >223), but the median synergistic ratio for 25
herbivores (3.6) was less than half the median for 15 entomophagous species
(8.4). The proportion of species with low synergistic ratios (below 4.8) was
significantly greater for herbivores (17/25) than for predators and parasites
(3/15). The median synergistic ratios for 13 crop pests (2.3) and 27
herbivores and non-herbivorous pests (4.2) were also significantly lower than
the median for entomophagous species. These findings contract the first part
of the preadaptation hypothesis. Considering the second part of the hypothesis, natural enemies
that have not been reported as resistant to insecticides had greater
synergistic ratios than several pests that are notorious for their ability to
evolve insecticide resistance. For example, the synergistic ratios for six of
seven species of parasitic Hymenoptera studied were higher than the ratios
for the German cockroach, corn earworm, fail armyworm and the southern house
mosquito. Thus, the data of Brattsten & Metcalf (1970) do not support the
idea that phytophagous pests have higher levels of detoxification enzymes
than natural enemies. Furthermore, their data suggest that low MFO activity,
as indicated by the synergistic ratio of carbaryl with poperonyl butoxide,
does not limit evolution of pesticide resistance. Pests with low synergistic
ratios have evolved resistance whereas natural enemies with relatively high
ratios have avoided resistance. These conclusions were recently confirmed by Strickler &
Croft (1985) in work that showed that piperonyl butoxide affected a predatory
mite (Amblyseius fallacis) more than its
herbivorous prey mite (Tetranychus
urticae). Additionally, the
synergistic ratio of piperonyl butoxide with propoxur for adults of the
ectoparasitic braconid Oncophanes
americanus (Weed) (14.0) was
8, 2 and 12-fold greater than the synergistic ratio for adults, large larvae
and medium larvae, respectively, of its herbivorous tortricid host, Artyrotaenia citrana (Fernald) (Croft &
Mullin 1984). The synergistic ratio for large larvae of the ectoparasite
(5.5) was more than triple the synergistic ratio for adults or medium larvae
of the host, but it was slightly less than the synergistic ratio of large
larvae of the host (6.0). Croft & Mullin (1984) stated that "synergist tests
are useful in qualitatively estimating the availability of an MFO
detoxification pathway," but they questioned the value of poperonyl
butoxide synergist tests as an indicator of MFO activity across diverse
arthropod species. Therefore, it is important to consider other measures of enzyme
activity, such as results from in
vitro assays. In vitro
inhibition studies and hydrolysis assays showed that lacewing larvae, C. carnea, have unusually active esterases that detoxify
pyrethroids (Ishaaya & Casida 1981). Although direct comparative tests were
not done, preparations of whole lacewing larvae were more active than larval
gut or integument preparations from an herbivore, the cabbage looper, Trichoplusia ni (Hübner). Lacewing larvae
were chosen for enzymatic tests because they have high natural tolerance to
pyrethroids and thus were suspected to have high esterase activity (Plapp
& Bull 1978). Consequently, the lacewing esterase activity data are a
biased sample of natural enemy detoxification enzyme capacity. Mullin et al. (1982) in a seminal study found in vitro detoxification enzyme differences between
susceptible strains of a predatory mite, Amblyseius
fallacis, and its
herbivorous prey, Tetranychus
urticae. MFO and
trans-epoxide hydrolase were higher in the prey than in the predator, but the
opposite was observed for cis-epoxide hydrolase and glutathione transferase.
Esterase activity was similar in susceptible strains of the two species. Even though the herbivorous mite had
higher activity than the predatory mite for an MFO enzyme (aldrin epoxidase)
and for trans-epoxide hydrolase, neither of these two enzymes were more
active in resistant than in susceptible strains of the herbivore. These data
suggest that resistance in the herbivore is not due to elevated levels of
aldrin epoxidase or trans-epoxide hydrolase. It appears, therefore, that
intrinsically higher levels of these two enzymes were not responsible for the
ability of the herbivorous pest to evolve resistance more readily than its
predator. On the other hand, of the five types of enzyme activity measured,
only glutathione transferase was higher in resistant prey than in susceptible
prey, which suggests that this enzyme could be partly responsible for
resistance in the prey species. Contrary to the expectation of a
preadaptation hypothesis, however, susceptible predators had more than
10-fold higher activity for this enzyme than did susceptible pests. It appears that the detoxification enzyme differences between A. fallacis and T.
urticae reported by Mullin
et al. (1982) do not support the second part of the preadaptation hypothesis.
It may be inappropriate to generalize from this case because predatory
phytoseiid mites are the one group of natural enemies that has readily
evolved pesticide resistance. Therefore, intrinsic disadvantages that slow
evolution of resistance in other natural enemies may be absent or diminished
in phytoseiids. Croft & Mullin (1984) compared various life stages of a
braconid ectoparasitoid, Oncophanes
americanus (Weed) and its
tortricid host, Argyrotaenia
citrana (Fernald). Based on
data from whole body preparations averaged across life stages, none of the
five in vitro assays conducted showed significantly lower enzyme
activity in the parasitoid compared to the host. Another in vitro
study comparing adult midgut levels of three types of enzyme between a
herbivorous coccinellid, Epilachna
varivestis Mulsant, and a
predatory coccinellid, Hippodamia
convergens Guerin-Meneville,
transepoxide hydrolase was virtually identical in the two species, but the
predator a four-fold higher cis-epoxide hydrolase activity and 2.5-fold
higher esterase activity than the herbivore (Mullin 1985). Thus this
comparison between taxonomically similar beetles that differ in feeding habit
does not support the first part of the pre-adaptation hypothesis. Aldrin epoxidase and trans-epoxide hydrolase activity were
lower in whole body preparations of Pediobius
foveolatus (Crawford), a
eulophid parasitoid, than in midgut tissues of its host, Epilachna varivestis
(Mullin 1985). Because enzyme activity of midgut tissue can be more than
200-fold greater than activity from a whole body preparation of the same
species (Croft & Mullin 1984), comparisons between activity in the midgut
of a pest vs. the whole body of a natural enemy are not a direct test of the
first part of the preadaptation hypothesis. A review of the aforementioned in vitro
studies of seven species and similar studies of four species of
piercing-sucking herbivores (Mullin 1985) shows broad overlap in
detoxification enzyme levels between herbivores and natural enemies. For
instance, aldrin epoxidase, trans-epoxide hydrolase, and cis-epoxide
hydrolase were lower in the herbivore Aphis
nerii Fonscolombe than in
any of the three natural enemies tested (A.
fallacis, O. americanus, and P.
fovelatus). Whole body
levels of aldrin epoxidase for the two species listed as chewing herbivores (T. urticae and A.
citrana) and the three
natural enemies tested fell within the range of the three aphid species
tested (A. nerii, Myzus persicae
(Sulzer), and Macrosiphus euphorbiae (Thomas). Perhaps the most detailed comparative study of detoxification
abilities was given by Yu (1987) who measured 15 components of enzymatic
detoxification capacity in the spined soldier bug, Podisus maculiventris
(Say), and four of its noctuid prey, Heliothis
virescens (Fab.), H. zea, Spodoptera
frugiperda, and Anticarsia gemmatalis (Hübner). In
vitro assays of midgut
tissues from adult predators and final instar larvae of the lepidopterous
prey showed that the predator lacked none of the detoxification enzyme
systems that were found in the prey. The prey had greater detoxification
capacity in 70% of pairwise comparisons between the predator and prey. For 11
of 15 components measured, either 3 or 4 of the prey species had greater
activity than the predator. However, the reverse was true for cytochrome
P-450, microsomal desulfurase, and glutathione transferase toward 1-chloro-2,
4-dinitro benzene (CDNB). Additionally, the proportion of the high-spin form
of cytochrome P-450, thought to indicate allelochemical-oxidizing capacity,
was higher in the predator than in any of the prey.. Topical bioassays showed
that the predator was generally more susceptible to organophosphorous and
carbamate insecticides, but was more tolerant of pyrethroids compared with
its prey (Yu 1988). However, the organophosphate tetrachlorvinphos was much
more toxic to two of the prey species, S.
fruigiperda and A. gemmatalis, than to the predator. Although penetration of
tetrachlorvinophos was slower for the predator than for S. frugiperda,
injection tests and acetylcholinesterase inhibition tests implied that the
predator's ability to survive tetrachlorvinphos was due to enhanced enzymatic
detoxification. Yu (1988) concluded that the predator's high pyrethroid tolerance
was probably due to reduced penetration or target site insensitivity. The in vitro assays of Yu (1987)
showing that the predator generally had lower enzymatic detoxification
capacity than its prey support the first part of the preadaptation hypothesis,
but several significant exceptions were also found. Later bioassays (Yu 1988)
show that patterns of susceptibility to insecticides could not be reliably
predicted on the basis of enzyme activities. Higher levels of certain
detoxification enzymes such as desulfurase, may actually increase the
toxicity of some insecticides. Available data from in
vivo and in vitro studies do not support the idea that natural enemies
have consistently lower levels of all types of detoxification enzymes than
pests, but this does not exclude the possibility of more subtle differences
between the two groups. For instance, an alternative hypothesis is that
oxidative detoxification enzymes are more active in pests than natural
enemies, whereas hydrolytic detoxification enzymes are similar in pests and
natural enemies (Plapp & Vinson 1977). The first part of this hypothesis,
however, is contradicted by data from in
vivo synergism tests and is
not strongly supported by data from in
vitro tests. Aldrin
epoxidase data from a predatory mite and its herbivorous prey (Mullin et al.
1982) support the hypothesis, but data from whole body preparations of an
ectoparasitoid and its lepidopterous host show the opposite trend (Croft
& Mullin 1984). Furthermore, intraspecific variation in MFO enzymes among
developmental stages sometimes even within an instar, can be greater than the
typical differences found between pests and natural enemies (Gould 1984,
Croft & Mullin 1984). Hydrolytic enzymes such as esterases and epoxide hydrolases
are often equally or more active in natural enemies compared with pests. Yu
(1987) found, however, that hydrolytic enzyme activities were lower in a
predator than in its prey in 88% of comparisons, but oxidative detoxification
activities were lower in the predator than the prey in only 59% of
comparisons. An obvious trend is that the ratio of trans- to cis-epoxide
hydrolase is, generally, higher for herbivores than natural enemies (Mullin
& Croft 1984). The lower trans/cis ratio of natural enemies, however,
does not explain their reduced ability to evolve resistance. The pests Blattella germanica and Myzus
persicae, both well known
for their ability to develop resistance, had lower trans/cis ratios than six
of seven entomophagous species studied (Mullin 1985). Nevertheless,
differences in trans/cis ratios and other biochemical differences might be
useful in designing selective pesticides (Mullin & Croft 1984, 1985). The detoxification enzymes found in pests are also present in
natural enemies. Data from in
vivo synergism tests show
that MFO enzyme levels in natural enemies were not consistently lower than
those in pests. In fact, evidence to data shows the opposite trend. Although in vitro enzyme assays have shown many cases in which pests
have higher levels of detoxification enzymes than natural enemies, the
reverse has been reported with nearly equal frequency. Therefore, the first
part of the hypothesis is not generally supported. In those cases in which
detoxification enzyme levels are higher in pests than in natural enemies,
there is little or no evidence indicating that this difference contributed to
more rapid evolution of resistance in the pest. Thus, there is little support
for the second part of the hypothesis. Finally, the differential
detoxification hypothesis does not address nonmetabolic resistance (such as
reduced penetration and target site insensitivity) or resistance in
nonherbivorous pests (Tabashnik 1986). Differences in
Intrinsic Tolerance.--The belief that natural enemies are intrinsically less
tolerant to pesticides than pests is, effectually, a generalized version of
the differential detoxification enzyme hypothesis. The concept is the same,
but unlike the differential detoxification hypothesis, the mechanism causing
the intrinsic difference is unspecified. Tests of this version of the
preadaptation hypothesis must determine (1) whether pests have higher
intrinsic tolerance to pesticides than natural enemies and if so then (2)
whether such intrinsic differences in tolerance cause natural enemies to
evolve resistance more slowly than pests. Two types of bias make it difficult
to evaluate the first part of the hypothesis. First, widespread resistance
and cross-resistance in pests can make it difficult to assess their intrinsic
tolerance. Inclusion of resistant pest populations in surveys of tolerance
would tend to inflate the tolerance of pests relative to natural enemies,
which are less likely to be resistant. Second, researchers may concentrate
efforts on pesticides that natural enemies can tolerate because such
compounds are particularly useful in integrated pest management. These two
biases operate in opposite directions, but their relative magnitude is not
easily determined. Brattsten & Metcalf (1970) studied the susceptibility to
carbaryl, finding that some pests were very tolerant (e.g., formicid ants).
However, median LD50 values did not differ significantly between
22 pests and 8 entomophagous species. Similarly, medians for carbaryl LC50
did not differ significantly between five pests. Surveys of studies, which
compared the LC50 or LD50 values within natural enemy/pest complexes, also do
not support the hypothesis that natural enemies are intrinsically more
susceptible to pesticides than are their prey or hosts (Croft & Brown
1975, Theiling & Croft 1988). Croft & Brown (1975) found that natural
enemies were more tolerant than their prey or host in 67 of 92 cases in which
the same bioassay method was used to compare species. Although predators were
usually more tolerant than their prey (63 of 77 cases), parasitoids were
usually less tolerant than their hosts (11 of 15 cases). Theiling & Croft (1988) calculated LC/LD50
ratios for 870 cases in which a natural enemy was compared to its prey or
host. Ratios ranged widely, yet natural enemies were more tolerant than their
prey or host in 57% of the cases. Furthermore, for 10 of 12 families of
natural enemies, including Braconidae and Aphelinidae, the average ratio for
the family showed that the natural enemy was more tolerant than its prey or
host. Phytoseiidae were as tolerant as their prey and only Ichneumonidae were
less tolerant than their hosts. These results contradict the differential intrinsic tolerance
hypothesis, but the authors of the reviews suggest some reasons why their
surveys may make natural enemies appear more tolerant than they actually are.
They note that LC/LD50 comparisons between pest/natural enemy
pairs are available for only a small subset of the studies of pesticide
impact on natural enemies. Natural enemies suspected to be tolerant to
pesticides may be more likely to be compared to their hosts or prey in
bioassays. Similarly, compounds thought to be more toxic to pests than
natural enemies may be more likely to be tested in comparative studies. Although some surveys suggest that natural enemies are not
consistently less tolerant to pesticides than pests, they often are.
Therefore, it is useful to consider how reduced intrinsic tolerance might
affect evolution of insecticide resistance. If ability to survive field rates
of pesticide is a criterion for resistance, then a natural enemy with lower
intrinsic tolerance would have to increase its tolerance more substantially
to be considered resistant. Tabashnik & Croft (1985) did some simulations which
suggest that under certain conditions reduced intrinsic tolerance could also
slow evolution of resistance as measured by changes in the frequency of a
resistance allele (R). Simulations based on a one locus model showed that 10
or 100-fold reduction in the LC50 of homozygous susceptible (SS)
individuals had little impact on projected times for resistance development
in natural enemies of apple pests. In contrast, reducing the LC50
of all three presumed genotypes (SS, RS, RR) by 10 or 100-fold greatly slowed
resistance development in nearly all cases. When the LC50's of all
three genotypes were reduced, heterozygous individuals were rendered
functionally recessive, which slowed evolution of resistance (Curtis et al.
1978, Taylor & Georghiou 1979, Tabashnik & Croft 1982). The
assumption of lower LC50's for all three genotypes implies that a
resistance allele increases the LC50 by a fixed multiple. Thus, if
the SS individuals are less tolerant, then so are RS and RR individuals.
Lowering the LC50 of SS individuals without altering the same of RS
or RR individuals assumes that a resistance allele provides a fixed level of
tolerance, regardless of the tolerance of SS individuals. In summary, surveys of comparative bioassay studies suggest
that on the average natural enemies are not intrinsically less tolerant to
pesticides than pests. Such surveys may be biased, however, and there are
many cases in which pests are intrinsically more tolerant than natural
enemies. Reduced intrinsic tolerance could retard evolution of resistance in
some natural enemies if resistance is defined as the ability to survive field
concentrations of a pesticide or if resistance alleles confer a fixed
multiple of increased tolerance relative to susceptible individuals. The
finding that Phytoseiidae, which are known for their ability to evolve
resistance, had low selectivity ratios compared to other natural enemies
(Theiling & Croft 1988) suggests that low intrinsic tolerance relative to
pests is not a major impediment to evolution of resistance in natural
enemies. The idea that natural enemies are not generally less tolerant to
pesticides than pests differs from widely held perceptions, which may be
based partly on observations that field applications of pesticides affect
natural enemies more than pests. However, disruption of natural enemy populations by field applications of
pesticides may be due to reduction of host or prey populations in addition to
direct toxic effects. Indeed, mathematical models show that if a pest and its
natural enemy are equally susceptible to a pesticide, the pesticide will have
a more severe impact on the natural enemy population than the pest population
(Wilson & Bossert 1971, Tabashnik 1986). Therefore, pesticide
applications can be extremely detrimental to natural enemy populations even
if the natural enemy's tolerance is similar to that of the pest. Differences in
Genetic Variation.--The genetic variation hypothesis maintains that natural
enemies evolve resistance more slowly than pests because natural enemy
populations have less genetic variation than pest populations (Huffaker 1971,
Georghiou 1972). Surveys of electrophoretic data show that Hymenoptera have
less variation in allozymes than most other insects. In particular the
expected heterozygosity or average gene diversity for 13 species of wasps was
less than half the expected heterozygosity for 158 species of Orthoptera,
Homoptera, Coleoptera, Lepidoptera and Diptera (Graur 1985). These data are
consistent with the idea that hymenopterous parasitoids have less genetic
variation than herbivorous insects. Although hymenopterous parasitoids have less allozymic
variation than most other insects, including many pests, this measure of
genetic variation may be unrelated to the ability to evolve insecticide
resistance. Some pests known for their resistance development had
high-expected heterozygosity (Heliothis
virescens = 0.389, H. zea = 0.327, Lygus
hesperus = 0.256) but others
had very low values (Blattella
germanica = 0.015, Myzus persicae = 0.000). The ability of some pests to readily
evolve pesticide resistance, even though they display little or no
electrophoretic heterozygosity, shows that this type of genetic variation is
not a prerequisite for resistance development. Genetic variation in tolerance to pesticides is required for
evolution of resistance, but it has rarely been measured (Roush &
McKenzie 1987, Tabashnik & Cushing 1988). How then can intrinsic
differences in genetic variation influence resistance development? Single
locus population genetic theory predicts that the rate of resistance
evolution increases approximately linearly as the logarithm of the initial
frequency of a resistance allele (May & Dobson 1986). In this sense large
differences in initial resistance allele frequency have relatively small
effects on rates of evolution. Most economically significant cases of
pesticide resistance are thought to be under monogenic control, but there are
also many examples of polygenic resistance (Roush & McKenzie 1987,
Tabashnik & Cushing 1988). According to quantitative genetics theory, the
rate of increase in pesticide tolerance would be directly proportional to the
additive genetic variance (Via 1986). Therefore, large differences in
additive genetic variance would have a major impact on resistance
development. Natural enemies (particularly parasitic Hymenoptera) may have
less allozyme heterozygosity than pests, but among herbivores this index of
genetic variation is not well correlated with the ability to evolve pesticide
resistance. The extent of genetic variation in pesticide tolerance in pest
and natural enemy populations is virtually unknown. Such variation could
influence rates of evolution of resistance, but the importance of this factor
cannot be assessed without more empirical information. Fitness Cost.--It is often
assumed that in the absence of pesticide a resistant individual is less fit
than a susceptible individual. If this fitness cost of resistance were
substantially greater for natural enemies than pests it might retard
evolution of resistance in natural enemies. Review of data available for
pests suggests that the fitness cost is generally not large, but it may
depend on the nature of the resistance mechanism (Roush & McKenzie 1987).
Little is known about the fitness cost of resistance in natural enemies.
Studies of the predators Metaseiulus
occidentalis and Chrysoperla carnea show little or no
fitness cost associated with resistance (Roush & Hoy 1981, Roush &
Plapp 1982, Grafton-Cardwell & How 1986), but data from other natural
enemies are needed to evaluate this hypothesis more completely (Croft &
Tabashnik 1989). Differences
in Population Ecology Underlying the population ecology hypothesis is that concept
that pesticide resistance evolves more readily in pests than natural enemies
due to differences in population ecology between them. Several specific
hypotheses are included in this general category: (1) resistance evolves more
readily in pests because natural enemies suffer from food limitation
following insecticide treatments (Huffaker 1971, Georghiou 1972); (2) differences
exist between pests and natural enemies in life history traits (Croft 1982,
Tabashnik & Croft 1985); (3) pests are more exposed to pesticides than
natural enemies (Croft & Brown 1975); and (4) pests have different
genetic systems than natural enemies (e.g., ploidy level). As with the preadaptation hypotheses, each hypothesis has two
parts (1) there is some difference in population ecology between pests and
natural enemies and (2) the difference enables pests to develop resistance
more readily than natural enemies. Food Limitation.--The food limitation hypothesis is based on the population
dynamics of interactions between natural enemies and pests (Huffaker 1971,
Georghiou 1972, Croft & Brown 1975, Tabashnik 1986). The idea is that the
few resistant pests surviving an initial pesticide treatment will have an
abundant food supply. In contrast, resistant natural enemies surviving
treatment will find their food supply (prey or host) severely reduced. Thus,
resistance evolves more slowly in natural enemies because they starve,
emigrate or have reduced reproduction following treatments that eliminate
much of their food supply (Tabashnik 1989). Pesticide treatments can reduce the food supply of natural
enemies while leaving the pests' food supply intact. Thus, there is little
question that pests and natural enemies differ in the way in which their food
supply is affected by pesticides. However, it is difficult to determine the
extent to which natural enemy populations are limited by the availability of
prey or hosts after pesticide treatments. Pesticide applications reduce
natural enemy populations, but in most cases, direct effects of the
pesticides on a natural enemy are confounded with indirect effects of the
pesticides on the natural enemy's food supply. Furthermore, the effect of
food limitation on a natural enemy's ability to evolve resistance cannot be
determined readily in the field. The food limitation hypothesis could be tested directly by
contrasting responses to pesticide treatments in a natural enemy population
feeding on a susceptible strain of a pest vs. a population of the same
natural enemy feeding on a resistant strain of the pest. The food limitation
hypothesis predicts that pesticide resistance will evolve in the latter case
but not the former. Although such a test has never been performed, there is
other experimental, historical and theoretical evidence available to evaluate
the food limitation hypothesis. If food limitation is a major factor slowing evolution of
resistance in natural enemies then it might be predicted that (1) natural
enemies will evolve resistance readily when provided with abundant food in
artificial selection programs; and (2) that if natural enemies can use food
sources that are not greatly reduced by pesticides (e.g., plants or resistant
pests), they will evolve resistance more readily than those that specialize
on susceptible pests. The successful laboratory selection for pesticide
resistance in natural enemies (Croft & Strickler 1983, Hoy 1985) provides
some support for the food limitation hypothesis, yet laboratory selection may
not produce high levels of resistance in natural enemies as readily as in
pests. Such differences are difficult to assess, but they could be due to
intrinsic limitations of natural enemies or to technical problems associated
with sampling, rearing and selecting large numbers of natural enemies. There is only one study that directly compared evolution of
pesticide resistance in a pest and its natural enemy in the laboratory. Croft
& Morse (1981) contrasted responses to selection for resistance to
azinphosmethyl in a predatory mite, Amblyseius
fallacis, and its prey, Tetranychus urticae. A susceptible strain
of the predator initiated from only a few individuals did not evolve
resistance after seven selections. However, a composite susceptible strain
initiated with 600 adult females from three predator strains, developed an
80-fold resistance in 22 selections. Another concurrent experiment with a
susceptible non-composite strain of the pest showed only a 20-fold increase
in LC50 in 22 selections. In the only experiment to compare
resistance development in the predator and prey with susceptible strains of
both species in contact, the composite strain of the predator evolved 80-fold
resistance whereas the pest strain evolved only a five-fold resistance. Such
results suggest that the pest did not develop resistance more readily than
its predator, but interpretations are complicated by several factors. First a
non-composite pest strain developed resistance more readily than a
noncomposite predator strain. Second, even though the proportional increase
in LC50 was higher for the predator than the pest in some
experiments, the final LC50 after selection was always higher for
the pest because of the pest's initially higher LC50. Third, the
food limitation hypothesis was not tested directly because predators fed on
leaf nectaries and survived even in the absence of prey. Therefore it was not
possible to determine if lack of food would retard evolution of resistance in
the predator. The ability of phytoseiid mites to derive nourishment from
plant materials and their ability to evolve resistance in the field
(Georghiou 1972, Croft & Brown 1975) is consistent with the second
prediction from the food limitation hypothesis. Also consistent with this
prediction is the general pattern that natural enemies usually become
resistant only after their prey or host develops resistance (Georghiou 1972,
Croft & Brown 1975, Tabashnik & Croft 1985). It was concluded that food limitation was not a key factor
affecting resistance development in Aphytis
melinus (Rosenheim & Hoy
1986). It was noted that a non-resistant host population can survive
pesticide applications if it is not contacted by treatments or if it is
naturally tolerant. Thus, treating the periphery of citrus trees with
dimethoate to control citrus thrips or with chlorpyrifos to control
orangeworms should not severely reduce populations of California red scale
which are distributed throughout the tree. Additionally, California red scale
populations are naturally tolerant of relatively low concentrations of
dimethoate used to control citrus thrips. Therefore, food limitation should
not restrict development of resistance to dimethoate or chlorpyrifos in Aphytis melinus. On the other hand, food limitation should slow
development of resistance in A.
melinus to carbaryl,
malathion, and methidathion because these insecticides are used to control
scales . An analysis of the range
in LC50's showed that resistance in A. melinus
to dimethoate and chlorpyrifos was not consistently greater than resistance
to carbaryl, malathion and methidathion. These results support the conclusion
that food limitation was not a major determinant of rates of resistance
development in the parasitoid. Rosenheim & Hoy (1986) noted that this is
a limited test of the hypothesis because many factors other than food
limitation (e.g., dross-resistance and variation among insecticides in the
duration and extent of use) could have affected the outcome. The potential impact of food limitation on the population
dynamics and ability to evolve resistance of natural enemies has been tested
with mathematical models. According to the Lotka-Volterra equations of
predator-prey population growth, equivalent mortality will suppress a
predator population more than its prey (Wilson & Bossert 1971). This
occurs because the predator's birth rate and the prey's death rate are
proportional to the product of the population sizes of both species. On the
other hand, the predator's death rate and the prey's birth rate are not
affected by the population size of the other species. Thus, a pesticide
treatment that kills 90% of predator and prey populations reduces the
predator's birth rate and the prey's death rate by a factor of 100, but
reduces the predator's death rate and the prey's birth rate only by a factor
of 10. More refined models also show that natural enemy populations are more
severely suppressed by pesticides than are pest populations, even though the
immediate mortality is similar for both populations (Waage et al. 1985). Considering whether the suppression of natural enemy
populations affects their ability to evolve resistance, May & Dobson
(1986) emphasized the general distinction between overcompensating and
undercompensating density-dependence. Pests generally rebound above their
long-term average or equilibrium levels following pesticide treatments and
thus show overcompensating density-dependence. On the contrary, natural
enemies recover slowly, showing undercompensating density-dependence.
Undercompensating density-dependence reduces the average population size,
thereby increasing the impact of immigration of susceptible individuals
(Comins 1977, Taylor & Georghiou 1979, Tabashnik & Croft 1982).
Therefore, in the presence of immigration, pests with overcompensating
density-dependence will develop resistance faster than natural enemies with
undercompensating density-dependence (May & Dobson 1986). Simulation studies of 12 natural enemies or orchard pests
showed that incorporation of a simplified version of the food limitation
hypothesis substantially improved the correspondence between predicted and
reported times for resistance development (Tabashnik & Croft 1985).
Natural enemies were assumed to begin evolving resistance only after their
prey or host had become resistant. Although the results supported the food
limitation hypothesis, this approach oversimplified dynamic ecological and
evolutionary processes. Other simulation studies included evolutionary
potential for resistance in both predator and prey, as well as coupled
predator-prey population dynamics (Tabashnik 1986). The key assumption of
these simulations was that low prey density reduced the predator's rates of
consumption, survival and fecundity. Predator functional response and the
effects of food shortage on predator survival and fecundity were partly based
on experimental data from mites (Dover et al. 1979). Even though the predator
and prey were assumed to have equal intrinsic tolerance and equal genetic potential
for evolving resistance, intensive pesticide use caused rapid resistance
development in the pest (prey), but either suppressed resistance development
or caused local extinction of the natural enemy (predator). These theoretical
results imply that food limitation is sufficient to account for pests'
ability to evolve pesticide resistance more readily than natural enemies. Pesticide treatments reduce the food supply of natural enemies
more than of pests. Severe reductions in food supply can slow resistance
development in natural enemies. Indirect support for the food limitation
hypothesis is provided by the success of laboratory selection programs in
which natural enemies are provided abundant food, by the general trend that
natural enemies evolve resistance only after their prey or host becomes
resistant, and by theoretical models. However, food limitation does not seem
to explain patterns of development of resistance to various insecticides in Aphytis melinus, a parasitoid of the California red scale. Life History
Characteristics.--Included
here are the number of generations per year,a the rate and timing of
reproduction, survivorship, development rate and sex ratio. Theoretical work
suggests that the rate of resistance development increases as reproductive
capacity increases, particularly the number of generations per year
(Tabashnik & Croft 1982, May & Dobson 1986). Historical patterns show
a positive correlation between the number of generations per year and rate of
resistance development (Tabashnik & Croft 1985, Georghiou & Taylor
1986, May & Dobson 1986). Variation in life history traits is sufficient
to explain variation in rates of resistance development among apple orchard
pests and their enemies (Croft &
Stickler 1983, Tabashnik & Croft 1985). If reproductive capacity,
especially the number of generations per year, is consistently higher for
pests than natural enemies, then this might explain why pests evolve
resistance more readily than natural enemies. This may be examined for 24 species of apple pests and natural
enemies (Tabashnik & Croft 1985). Although the average number of
generations per year was slightly higher for pests than natural enemies,
there was also a broad overlap. Seven of 12 pest species had less than three
generations yearly, but only five of 12 natural enemies had fewer than three
generations per year. Generations per year ranged widely for each group. Thus
no consistent difference between pests and natural enemies in generations per
year is evident. The apple arthropods may be a biased sample because such a
high proportion of the natural enemies have developed resistance. Broad
surveys of fecundity in parasitic Ichneumonidae and Tachinidae show a range
from 20 to 5000 eggs per female within these groups (Price 1984). Exposure.--Rate of resistance development is a function of selection
intensity, which is determined in part by the extent of exposure to
pesticides. Croft & Brown (1975) hypothesized that natural enemies are
often less intensively selected than pests because pesticides are directed at
pests; natural enemies contact pesticides only because they occupy the same
habitat as their prey or host. However, mobile predators and parasitoids
might contact more toxicant and thus suffer greater mortality from residual
deposits than would sedentary pests in the same habitat (Croft & Brown
1975). Genetic Systems.--Evolutionary considerations about pesticide resistance are
generally based on the assumption that organisms are diploid and sexually
reproducing, but insects and mites have a variety of genetic systems.
Differences in such systems between pests and natural enemies could influence
their relative ability to evolve resistance. For instance, many parasitic Hymenoptera
are haplo-diploid. In a modeling study, however, resistance evolved faster
under haplo-diploidy than diplo-diploidy (Horn & Wadleigh 1987). Thus,
haplo-diploidy does not seem to be a factor slowing evolution of resistance
in parasitic Hymenoptera (Related Research). Various genetic systems are known in phytoseiid predatory
mites, including thelytoky, parahaploidy (embryos of both sexes are diploid,
but males lose one chromosome set during embryonic development), and
something akin to arrhenotoky (unfertilized eggs produce haploid males,
fertilized eggs produce diploid females) (Hoy 1985). Parahaploid phytoseiids
such as Metaseiulus occidentalis and Phytoseiulus persimilis Athias-Henriot may
have some advantages of both haploidy (exposing haploid individuals to
selection) and diploidy (recombination) (Hoy 1985). This might explain why
phytoseiids evolve resistance to pesticides more readily than other natural
enemies, but it does not support the idea that the genetic systems of natural
enemies retard their resistance development. Other factors that could affect evolution of resistance in
pests and natural enemies are the extent of sexual vs. asexual reproduction,
inbreeding and coloniality. Colonial insects would not be expected to evolve
resistance readily because they have small effective population size (few
reproductives), slow generation turnover, and their reproducing individuals
usually have limited exposure to pesticides. These factors may explain the
paucity of documented cases of resistance in social Hymenoptera and Isoptera
(Georghiou 1981), many of which are pests. However, they do not explain the
lack of resistance in nonsocial parasitic Hymenoptera. Genetic systems and
related factors may influence resistance development in pests and natural
enemies, but it does not seem that there are consistent differences in these
traits that would favor resistance development in pests compared to natural
enemies. Arthropod
Resistance to Pesticides (Van Driesche & Bellows (1996) Account) -------------------------------------------------------------------------- Effects of Plant Properties on
Natural Enemies -------------------------------------------------------------------------- Van Driesche & Bellows (1996) observed that pesticide
resistance develops in a population when certain individuals possess genes
which allow them to better avoid or survive contact with pesticides. Treating
such a population with a pesticide confers differentially greater survival or
fitness on these tolerant individuals, and the frequency of the resistant
genotype increases when the tolerant individuals reproduce. For species in
which these surviving individuals remain together as a new breeding group,
undiluted by addition of susceptible individuals from outside the
pesticide-treated area, pesticide resistance may develop. An increasing
number of pests of several types have become resistant to pesticides. When
pests develop resistance, agriculturists may respond by increasing dosage,
changing or alternating pesticides, or combining several pesticides. If
resistance is sufficiently severe to prevent control of the pest, chemical
control may be abandoned and management systems based on biological control,
including the conservation of native natural enemies, may finally be
implemented instead. On the other hand, when natural enemies develop
resistance to pesticides commonly used on a crop, this resistance may make it
possible to conserve such natural enemies as important mortality agents
contributing to the control of pests in crops even with continued pesticide
use. Pesticides can reduce natural enemy effectiveness either by directly
causing mortality or by influencing the behavior, foraging, or movement of
natural enemies, their relative rate of reproduction compared to that of the
pest, or by causing imbalances between host and natural enemy populations
such as catastrophic host synchronization (Table 7.1) (Jepson 1989; Waage
1989; Croft 1990). Many classes of pesticides are directly toxic, to one degree
or another, to some categories of natural enemies. Insecticides and
acaricides, for example, are likely to be damaging to most parasitoids and
predacious anhropods (Bartlett 1951, 1953, 1963, 1964b, 1966; Bellows and
Morse 1988, 1993; Bellows et al. 1985, 1992a, 1993; Morse and Bellows 1986;
Morse et al. 1987), while fungicides would generally not affect these
organisms but may inhibit fungi pathogenic to pest arthropods (see Yasem de
Romero 1986; Saito 1988; Majchrowicz and Poprawski 1993) or fungi
antagonistic to plant pathogens (Vyas 1988). Agricultural chemicals such as
soil sterilants drastically alter soil microbial, fungal, and invertebrate
communities, affecting the influence of such soils on plant pathogens. Other
materials may be toxic outside of their intended scope of use, A bird
repellent, for example, may also be insecticidal. A fungicide may also kill
arthropods (sulfur is damaging to phytoseiid mites) or affect their
reproduction or movement. Herbicides may kill beneficial nematodes applied
for insect control (Forschler et al. 1990). It is thus important to assume
that any pesticide, of whatever type, might affect a natural enemy until data
are available to demonstrate that it does not (Hassan 1989a). Even materials
often thought of as nontoxic, such as soaps or oils, which may be safe to
humans, may be harmful to natural enemies. Oils may reduce the emergence of
parasitoids of scale insects as well as cause scale mortality (Meyer &
Nalepa 1991). The degree of effect on a natural enemy population caused by
any given pesticide will depend on both physiological and ecological factors.
Physiological selectivity consists of the intrinsic relative toxicities of
the compound to the pest and the natural enemy. Chemicals vary greatly in
their inherent toxicity to a species (Jones et al. 1983; Smith & Papacek
1991). Some insecticides or acaricides have been found that are effective
against pests and also mostly harmless, physiologically, to some arthropod
natural enemies. Toxicity varies with species of natural enemy, but some
examples include primicarb, toxins of Bacillus thuringiensis,
fenbutatin oxide, and diflubenzuron (Hassan 1989a); certain plant alkaloids,
mevinphos, and cryolite (Bellows et al. 1985; Bellows & Morse 1993);
avermectin and narrow range oils (Morse et al. 1987); and the systemic
materials demeton and aldoxycarb (Bellows et al. 1988). Ecological
selectivity results from those aspects of the use of the material that
determine the degree of contact that actually occurs between the pesticide
and the natural enemy (Van Driesche & Bellows 1996). Contact is affected
by the formulation and concentration applied, the persistence of the material
in the environment (as affected by such abiotic factors as temperature and
rainfall), the mode of action of the chemical (contact vs. Ingestion), the
spatial pattern of application, and the timing of application (Van Driesche
& Bellows 1996). Effects
of Plant Properties on Natural Enemies The characteristics of plants influence natural enemies in a
wide range of ways, some of which are just beginning to be recognized. It is common
for a particular host species to be subject to varying levels of attack by
natural enemies when it feeds on different plant species. Plant features
influence foraging success and reproductive fitness of natural enemies.
Knowledge of such interactions is important for conducting foreign
exploration (to obtain species or strains of natural enemies adapted to
attack the target pest on the target crops); for planning conservation and
augmentation programs; and for guiding changes made to crop plants through
plant breeding (so that natural enemy action is enhanced rather than reduced
during creation of new crop varieties, (see Boethel and Eikenbary (1986).
Strong et al. (1984) scussed relationships between plants and insects and
concluded that competition for space from natural enemy attack was important
in shaping herbivore communities. Price (1986) presented a classification of
how plants can affect natural enemies through either semiochemically mediated
effects, chemically-mediated effects, or physically-mediated effects. In some instances, plant compounds are used directly by
natural as cues for habitat location. In other instances, plant compounds may
either be hidden by herbivores or may be released by plants under herbivore
attack, resulting in the attraction of natural enemies directly to the host.
At the level of plant communities, associated plants may produce compounds
that either enhance attractiveness to natural enemies or may make the
detection of host plants by natural enemies more difficult (Van Driesche
& Bellows 1996). Chemically mediated effects of plants on natural enemies
include the use by natural enemies of plant products such as nectar and
pollen as food sources. Nutritional qualities of plants also affect natural
enemies indirectly by influencing the rate of growth and survival of
herbivores which feed on them. Herbivores, which develop on plants of reduced
nutritional quality, are likely to require a longer period to develop and may
remain in stages susceptible to natural enemy attack longer than herbivores
developing on more nutritious hosts. Plant qualities that cause mortality to
an associated herbivore affect rates of the herbivore's survival in its
various life stages. This in turn will affect the survival of immature
parasitoids associated with the stage of the herbivore, and also will affect
the number of hosts in subsequent stages that are available for other
parasitoids or predators to attack (Van Driesche & Bellows 1996).
Finally, plant compounds may be sequestered by herbivores and used as
defenses against natural enemy attack. Protection of monarch butterflies
(Danaus plexippus (L.)) from predation by birds through sequestering by
monarch larvae of plant-derived cardiac glycosides is a well-known example
(Brower 1969). Physical aspects of plants may affect natural enemies in
several ways. Spatial dispersion of plants can affect the ability of
herbivores and natural enemies to locate and, in some cases, successfully
colonize the plants. Plant structures can provide herbivores with physical
protection. Insects in the centers of large fruits or galls, for example, are
less accessible to parasitoids with short ovipositors. Some plant features
may directly shelter natural enemies. Domatia (pits and pockets) on leaves
are used by phytoseiids and plants with such features harbor higher numbers
of these predatory mites (Walter and O'Dowd 1992; Grostal and O'Dowd 1994). Plant festures
such as leaf toughness or hairiness, which in some cases defend plants
against herbivores, may also affect natural enemies. Increased trichome
density on leaves is associated with reducing walking speed and lowered rates
of foraging, making some natural enemies less effective in finding hosts (Hua
et al. 1987). Some predators, such as chrysopid larvae, may also experience
reduced walking speed on hairy leaves (Elsey 1974), but other predators, such
as larvae of the coccinellid Adalia bipunctata, forage for prey more
effectively on leaves with single scattered hairs, versus glabarous, waxy
leaves. This because hairs force more frequent thrning and cause the larvae
to move across the leaf surface rather than to only follow the veins and leaf
edge (Shah 1982). Some phytoseiids have been found to be more abundant on
grape varieties with hairy undersides, perhaps because of more favorable
microclimate and protection from rain (Duso 1992). The influence of leaf
pubescence on entomophagous species was reviewed by Obrycki (1986). In a
broad sense, the shape of plant leaves and the arrangement of branches and
other plant parts affect how natural enemies structure their foraging on the
plant and between sets of plants (Ayal 1987; Grevstad & Klepetka 1992).
Coccinellid larvae of several species, e.g., drop off leafless pea plants (Pisum
spp.) Less frequently than from normal plants because tendrils of leafless
plants are easier for beetles to grasp (Kareiva & Sahakian 1990). Plant
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