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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 sublethal 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
canopies in which leaves overlap are associated with increased rates of
dispesal of coccinellids, in the absence of prey, than crops in which plant
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