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EXPERIMENTAL
DESIGN & SAMPLING
I. Luck et al. (1999)
emphasized that in order to improve success rates in biological control, an understanding
of events in past successful
introduction programs is essential. A.
Successful cases can be used to test hypotheses about predator/prey
interactions, and develop criteria for identifying effective natural
enemies. B. Van
Driesche et al. (1991) reviewd the analytical bases developed in the late
1980's to estimate total losses from parasitism. Thay stated that, "Because the population of an insect
stage typically begins to lose members through death or development to the
next stage in the life cycle before the entire recruitment to the stage is
completed, at no time are all members of the generation present to be
counted. This idea is analogous to a
sink partly filled with water (i.e., the population), into which water is
flowing (recruitment) and from which water is draining (death or advancement
to the next stage)..." "To
construct a life table, we need to know the total numbers that enter a stage
(in this analogy, the total amount of water entering the sink). C. What
biologists typically measure, however, is the number of animals present per
sample unit at points in time (which is analogous to the amount of water in
the sink at any given time). Although
it is true that the volume of water present at any time is determined by the
moment-to-moment balance of cumulative influx minus cumulative outflow, if
these latter quantities are not known, it is not possible to determine total
inflow from even the most detailed set of observations on the quantity of
water in the tank at fixed moments in time.
What is needed is a continuous record of recruitment for the whole
period over which animals enter the stage of interest for the
generation. This can be achieved by
measuring recruitment for a series of contiguous intervals spanning the whole
period when recruitment occurs (e.g., Van Driesche & Bellows 1988)." D. Van
Driesche et al. (1991) continued, "When the goal is to assess not only
how many insects enter a given life stage over the course of a generation,
but also to determine how many of that number subsequently become
parasitized, the problem is compounded because the basic problem discussed
above now applies to two quantities that must be measured; i.e., the total
number of hosts recruited and the number that subsequently become
parasitized. The linkages between
these value are both dynamic and complex..." "Although there are some systems in which biology and life
history characteristics are such as to produce nondynamic systems not subject
to these problems (for example, cases where the sampled stage is in a
diapause stage and accumulates without loss as, for example, is approximately
the case for gypsy moth eggs, because dead or parasitized eggs remain
countable) or systems such as some leafminers in which lost insects continue
to be traceable in samples through their remains, the majority of insects do
have overlapping recruitment and losses.
For these cases, densities and percentage parasitism values seen in
samples do not measure adequately the level of parasitoid effect." II. Approaches in the evaluation process
include 1. life table analysis, which is a descriptive method; 2.
stage frequency
analysis; 3. direct measurement of recruitment; 4. death rate analysis; 5. experimental manipulations in the
field.
A. The primary goal is to determine
whether regulation of the host population exists and to identify the agents responsible for regulation. B. Luck
et al. (1999) defined regulation as the biological processes involving
natural enemies that suppress prey or host densities below levels that
prevail in the absence of natural enemies.
It must be determined whether the populations are regulated, measure
the level of regulation and identify the forces involved in regulation. If the populations are not regulated, if
the regulation is intermittent, or if the level of suppression is inadequate,
then other options to consider are (1) introduction of additional natural
enemies, (2) inoculative or inundative releases, (3) development of plant
resistance, (4) change the cultural practices, etc. C.
There are other key references pertaining to measurement of natural
enemy impact (Thompson 1955, Richards et al. 1960, Hafez 1961, Kirtitani
& Nakasuji 1967, Manly 1974, 1976, 1977, 1989; Ruesink 1975, Russell
1987, Kolodny-Hirsch 1988, Schneider et al. 1988, Van Driesche 1988, Bellows
et al. 1989, Gould et al. 1989,
Keating 1989, McGuire & Henry 1989, Van Driesche et al. 1989, 1991a,b,
Buonaccorsi, J. P. & J. S. Elkinton 1990, Gould, J. R. 1990a,b, Hazzard
et al. 1991). III. There is probably no
single method which can provide conclusive evidence that natural enemies are
regulating a population. A.
Natural enemies are not the only factor involved in many interactions,
and the plant can significantly affect the natural enemies' ability to
regulate (Flanders 1942, Starks et al. 1972, Price ta al. 1980). B. Luck
et al. (1999) conclude that no research method if free of technical problems,
and management decisions are made with insufficient knowledge. Therefore research aimed at developing an
integrated pest management program is a continuous process in which
hypotheses are continually being refined and tested (Way 1973). Classical biological control and
augmentive biological control are important IPM tactics, but they must be
pursued and expanded to include situations for which they have not ben
emphasized (DeBach 1964, 1974, Ridgway & Vinson 1976, Carl 1982). Indigenous biological control forms the
foundation for pest management and therefore must be utilized if IPM is to
become more effective. Its presence
in an agroecosystem can be demonstrated by disrupting it with insecticides
(Folsom & Brondy 1930, Woglum et al. 1974, Brown 1951, Pickett & Patterson
1953, Ripper 1956, Bartlett 1968, Smith & van den Bosch 1967, Wood 1971,
Ehler et al. 1973, Eveleens et al. 1973, Croft & Brown 1975, Luck &
Dahlsten 1975, Luck et al. 1977, Reissig et al. 1982, Kenmore et al. 1984),
or by comparing unsprayed, abandoned orchards with treated orchards. Insecticidal disruption provides one of
the best experimental techniques for evaluating natural enemies. It can reveal the amount of control
provided by indigenous entomophages (Stern et al. 1959, Smith & van den
Bosch 1967, Falcon et al. 1968, MacPhee & MacLellan 1971, Wood 1971,
Flint & van den Bosch 1981, Jones 1982, Metcalf & Luckmann 1982,
Kenmore et al. 1984).
C. In the experimental
evaluation of biological control, testing whether regulation exists and which
natural enemies are
responsible for the regulation, life tables and their analyses provide
a quantitative framework in which to explore the consequences of a
predator/prey interaction and to generate hypotheses. However, life tables cannot demonstrate
the efficacy of natural enemies in
suppressing a host or prey population in the field; only experimental methods
can do this (Luck et al. 1999). Some
populations cannot be
manipulated with available technology because they are based on untested
assumptions. Evidence is that natural
enemies
suppress host/prey populations and experimental results suggest that a host
plant's nutritional quality, its physical structure
and its chemical defenses play a role in pest suppression (Denno &
McClure 1983, Futuyma & Peterson 1985, Whitham et al. 1984,
Mattson 1980). IV. The development of an appropriate sampling
routine is essential for the evaluation of natural enemies. A. The
design is determined by the objectives of the experiment, the biology of the
organisms involved and the cost of acquiring the information to meet the
objectives. The sampling procedure used
to acquire data and the statistical techniques used to analyze data must be
decided before field evaluation begins.
B.
Appropriate experimental designs require preliminary studies to
identify variation sources.
Preliminary samples can save time and resources (Green 1979). For example Legner (1979, 1983, 1986) and
Van Driesche (1983) described some of the problems associated with estimating
and interpreting percent parasitism from field samples, while Van Driesche
& Bellows (1988) discussed analytical procedures for dealing with some of
the problems. C.
Statistical randomness is important in population sampling and in the
assignment of treatments. Randomness
includes locating field plots and selecting sample plants and sample
units. Each sample unit must have an
equal chance of being selected.
Nonrandom sampling makes analysis of the data questionable because of
the uncertainty associated with the estimation of the values. Texts and articles on sampling and
experimental design should be consulted before an evaluation of natural
enemies or of biological control is begun (Morris 1955, 1960, Cochran 1963,
Stuart 1976, Elliot 1977, Jessen 1978, Southwood 1978, Green 1979). V. Evaluation in biological control must
consider the following: Do natural
enemies affect pest population densities; what natural
enemies kill a pest; how quickly will an natural enemy kill a pest;
how many pests will a natural enemy kill; how does an natural enemy
respond to changes in pest densities in the field; and how do environmental
changes affect the predator-prey/parasitoid- host
interaction (Luck et al. 1999). A. When
evaluating indigenous natural enemy populations, it is necessary to determine
whether biological control of the hosts exists. B. An
effective means compares pest densities in an area not treated with
pesticides to pest densities in an area subjected to traditional pesticide
practices. Ceasing the use of
pesticides in parts of a field does not constitute a previously unsprayed
area, as prolonged pesticide use reduces natural enemies and alternate prey
or hosts upon which the natural enemies depend. C. Time
is required to reestablish interactions between natural enemy and prey/host
populations. D.
Also, the untreated area must be large enough to buffer the plots from
pesticide drift and to insulate arthropod populations within from the
dynamics and interactions of those in the adjacent areas. Estimating the degree of regulation
exerted by the natural enemies residing in plots subjected to disruptive
effects almost always underestimates the amount of potential biological
control (Luck et al. 1999). Pesticide
trials in which a small untreated block within a sprayed area is used to
estimate the amount of control from factors other than the pesticide
treatments are not adequate in that populations in the unsprayed area are
overwhelmed by the dynamics of those in the surrounding treated blocks. VI. Techniques For Evaluation
A. Introduction / Augmentation
of Natural Enemies.--In
classical and indigenous biological control, a prey population is expected to
be self sustaining. Control derived from
augmentive releases is only temporary, lasting one season or less. The evaluation of each method poses
different problems. In Classical
biological control a natural enemy's impact can be demonstrated by comparing
the change in a pest's density in the initial release sites with a control
site of similar characteristics but lacking the natural enemy (Huffaker et
al. 1962, Legner & Silveira-Guido 1983).
A drop in the pest's abundance in the release site compared with the
control site suggests that the natural enemy is responsible for the pest's
decline. This conclusion is further
supported if the pest's density in the control site also declines following
the subsequent introduction or immigration of the natural enemy to that
site. Replication of release and
control sites adds confidence to the evaluation if the pattern of decrease is
consistent across the experimental plot.
A similar design can evaluate augmentive releases, but the results may
be confounded if closely related or morphologically similar indigenous and
released natural enemies attack the same pest (see Legner & Brydon
1966). However, Oatman & Platner
(1971, 1978) showed that release and control plots are never identical
ecologically. Exclusion, inclusion or
interference methods are required to assess the difference between resident
and released natural enemies.
Introducing genetically marked individuals that differ from the
resident population only in the genetic marker can also distinguish between
resident and introduced populations (Legner et al. 1990, 1991; Luck et al.
1999). The translocation of natural enemies to areas
invaded by pest species and subsequent classical biological control gives
additional proof that indigenous natural enemies can have a significant role in
regulation of native populations (Wilson 1960, Dowden 1962, McGugan &
Coppel 1962, McLeod 1962, DeBach 1964, CIBC 1971, Greathead 1971, Laing &
Hamai 1971, Rao et al. 1971, Clausen 1978, Luck 1981, Kelleher & Hulme
1984, Cock 1985). Further proof is given
when the introductions are repeated at several locations with similar results
(DeBach 1964, Laing & Hamai 1976). B. Exclusion / Inclusion of Natural
Enemies.--Cages and other
barriers have been used in exclusion and inclusion procedures to evaluate natural
enemies (Smith & DeBach 1942, DeBach et al. 1949, DeBach 1955, Sparks et
al. 1966, Lingren et al. 1968, Way & Banks 1968, van den Bosch et al.
1969, DeBach & Huffaker 1971, Ashby 1974, Campbell 1978, Richman et al.
1980. Aveling 1981, Faeth & Simberloff 1981, Frazer et al. 1981b, Jones
1982, Elvin et al. 1983, Chambers et al. 1983, Linit & Stephen 1983,
Barry et al. 1984, Kring et al. 1985).
Cages to exclude natural enemies were first deployed by Smith &
DeBach (1942), using paired sleeve cages to test whether the introduced
parasitoid Metaphycus helvolus (Compere) regulated
the black scale, Saissetia oleae (Bern.). Comparison of the black scale in the open
and closed cages showed that less black scale survived in the open
cages. This technique was modified by
using insecticide impregnated netting to kill natural enemies that emerged in
the closed cages when the methods was used to evaluate other classical
biological control projects (DeBach et al. 1949, DeBach 1955, DeBach &
Huffaker 1971). 1. Cages with different sizes of mesh have
been used to exclude natural enemies based on their size (Campbell 1978,
Kring et al. 1985). Three types
employed were (1) a complete exclusion cage with small mesh netting and
sealed at both ends, (2) a control cage with similar netting and open at both
ends and (3) a partial exclusion cage with large mesh netting and closed at
both ends. The latter excluded large
predators but allowed access of small predators and parasitoids. 2. Sleeve and field cages with more complex
designs, such as those which enclosed whole plants, accompanied by samples of
the prey and natural enemy populations, showed that the spring increase of
predators eliminated black bean aphid, Aphis
fabae Scop., colonies on its
overwinter host, Euonymus europaenus L., after June (Way
& Banks 1968). If spring aphid
populations had been dense on the tree, the predators that remained after the
aphids emigrated to their summer hosts prevented recolonization of spindle
tree by late fundatrices during the summer, even though the spindle tree was
capable of supporting an increasing aphid population. Closed field cages covered with dieldrin
treated netting coupled with hand removal excluded natural enemies from some
spindle trees whereas open field cages constructed with slatted walls allowed
access of the natural enemies to the aphids on the uncaged trees but provided
the same degree of shading as the closed cage (Way & Banks 1958,
1968). Such experiments and making
census of populations on the sample twigs document the importance of
predators in excluding aphids from the overwintering host plant during the
summertime (Luck et al. 1999). 3. The evaluation of indigenous natural
enemies of cereal aphids was done in large field cages and accompanying
population samples. The experimental
design combined field cages erected at several intervals after the aphids
immigrated into a winter wheat field.
The growth rates and peak densities of the aphid populations within the
cages was compared with those in several open plots of similar size (Chambers
et al. 1983). Samples showed that the
abundance of Coccinella 7-punctata L. was negatively
correlated with aphid abundance in the open plots but the incidence of
parasitism and disease was not negatively correlated with aphid
abundance. These latter two factors
were more common in the caged plots.
If the difference between the aphid densities in the cage and open
plots was converted to per capita aphid consumption, based
on the sampled coccinellid densities, the calculated values were within the
range of known values. Coccinellids
appeared to be the key agents limiting the growth rate and peak abundance of
cereal aphids during mid season but they were unable to do so early in the
season (Rabbinge et al. 1979, Carter et al. 1980). 4. Field cages with open field controls were
used to determine whether the predator complex aggregated at dense patches of
the pea aphid, Acrythosiphon
pisum (Harris) (Frazer et al.
1981b). The cages excluded the
predators and allowed the aphid population to increase to about 5X that of
the open control plots. When the
cages were removed the aphid populations declined to the densities that
prevailed in the control plots and the decline was correlated with increased
predator numbers aggregating at the denser aphid patches. Large field cages have also been used to
evaluate the potential of predators in cotton to reduce egg and larval
populations of the tobacco budworm, Heliothis
virescens (F.) (Lingren et
al. 1968). Evening releases of
budworm moths initiated the prey populations within the cages. Fewer prey survived in the cages with
predators than in cages excluding predators.
Similar studies were conducted in California cotton to evaluate
predation on the survival of larval populations of the cotton bollworm, Heliothis zea (Boddie) (van den Bosch et al. 1969). The cotton plants within the predator-free
cages were treated with an insecticide to eliminate resident predators before
bollworm larvae were introduced.
Significantly fewer prey survived in the untreated cages and
significantly more predators were collected from the untreated cages.
5. In order to determine
whether indigenous natural enemies or microclimatic changes within a cage
explained the increased survival of caged European corn borer, Ostrinia nubialis (Hübner) larvae, caged and uncaged plots and
plots of similar size but enclosed with a cage within a cage were used
(Sparks et al. 1966). The double
cages was designed so that the screened panels on the inside cage were
opposite that unscreened panels on the outside cage and vice versa. This arrangement allowed predators access
to the plants inside while maintaining the same level of shading and air flow
in both the complete cage and cage within a cage plots. Entomopathogenic fungi (Deuteromycotina)
effects were also tested with cages for the black bug, Scotinophara coarctata
F., in rice (Rombach et al. 1986a.).
Adult bugs were introduced into screened cages and applications of
fungi Beauveria bassiana (Bals.) Vuill, Metarhizium anisopliae (Metsch.) and Paecilomyces lilacinus Thom. were made with
a backpack sprayer. The black bugs
were significantly less abundant in all treatments when compared with
untreated controls, with effects lasting to nine weeks. Similarly caged brown planthoppers, Nilaparvata lugens Stal, were treated with
entomopathogenic hyphomycetes (Fombach et al. 1986b). Mortality from fungal infections ranged
from 63-98% three weeks after application.
6. Ground predators,
principally carabids, were excluded with trenches that contained insecticide
soaked straw, from the cabbage root fly, Erioischia
brassicae (Bouché) (Wright
et al. 1960, Coaker 1965). Polythene
barriers were used to exclude predators from two of three treatments in which
the predator density was manipulated to determine its effect on the density
of aphid populations (Winder 1990).
Sticky bands around selected branches of a spindle tree were used to
exclude the walking predators of Aphis
fabae (Way & Banks 1968)
and around the plant base to exclude walking predators of Trichoplusia ni (Hübner) (Jones 1982).
Sticky circles around Trichoplusia
ni eggs were used to exclude
predators and parasitoids from attacking the eggs (Jones 1982).
7. Studies relating cage
densities to the densities of resident field populations of predators outside
the cages have been used for aphids and Lepidoptera (Frazer & Gilbert
1976, Campbell 1978, Aveling 1981, Frazer et al. 1981b, Chambers et al.
1983), providing useful hypotheses (Way & Banks 1968, van den Bosch et
al. 1969, Campbell 1978, Carter et al. 1980, Aveling 1981, Faeth &
Simberloff 1981, Frazer et al. 1981b, Chambers et al. 1983). Cages can provide quantitative information
on predation rates (Elvin et al. 1983) but not without limitations. Small sleeve cages inhibit predator or
prey movement and are good for experiments with sessile species or species
with low vagility (smith & DeBach 1942).
The abundance of citrus red mite, Panonychus
(= Metatetranychus) citri (McG.), within sleeve
cages was sometimes 12X greater than outside sleeve cages (Fleschner 1958)
even though the mite population outside the cages was kept predator-free by
continuous hand removal of predators.
It was thought that the cage prevented the reproductive females from
emigrating, that the microclimate within the cages favored rapid growth of
the mite population, or both factors influenced population growth (Fleschner
et al. 1955, Fleschner 1958).
8. It is not possible to
identify which members of a predator/parasitoid complex are regulating a host
population with exclusion cages unless the complex consists of one or a few
species (Jones 1962). Partial exclusion
cages may show whether small predators, pathogens or parasitoids regulate in
the absence of large predators, but they cannot show whether large predators
regulate prey in the absence of parasitoids or small predators (Luck et al.
1999). Cages may also inhibit
predator or prey movement or interfere with natural enemy oviposition. Two leaf mining species on oak failed to
reproduce within whole tree cages and a third species failed to reproduce in
one cage (Faeth & Simberloff 1981).
Aphid alates cannot emigrate from a cage, thus caged versus uncaged
aphid populations may show differences in density because alate immigration
reduces the uncaged aphid population.
Some predator species aggregate at patches of high prey density in a
numerical response (Readshaw 1973, Frazer et al. 1981a. Kareiva 1985). Such behavior may be inhibited by cage
size because the spatial pattern in nature to which the predator species
responds is larger than that present within the cage. Also, confining predators to a cage may causae
them to search areas more frequently and thereby increases the likelihood
that they will encounter prey. Under
these conditions the predator may reduce prey densities to levels below
normal, and in this way inclusion studies resemble laboratory experiments in
which predators are confined with prey (van Lenteren & Bakker 1976, Luck
et al. 1979).
9. Erroneous interpretations
can result when prey are placed into a cage without consideration of their
preferences for oviposition sites, their density and distribution patterns or
their preferred feeding sites under field conditions. Some predators and parasitoids use
kairomones to find their prey and hosts (Hassell 1980, Nordlund et al.
1981). Some kairomones are associated
with feeding activity. Placing prey
or hosts in new sites influences their risk of detection. Food quality may affect a phytophage's
feeding time and increase its risk to predation because of the kairomones
released while feeding (Nordlund et al. 1981). Detailed studies of a predator's searching behavior and capture
rates and a prey's oviposition and feeding behavior are important (Fleschner
1950, Dixon 1959, Frazer & Gilbert 1976. Gilbert et al. 1976, Rabbinge et
al. 1979, Carter et al. 1980. Baumbaertner et al. 1981, Frazer & Gill
1981, Sabelis 1981).
10. Whenever predator free
controls are employed, it is difficult to exclude all predators, even when
they have been treated with insecticides (van den Bosch et al. 1969, Irwin et
al 1974, Elvin et al. 1983). Some
predators may pass through excluding screens when in small developmental
stages (Sailer 1966, Way & Banks 1968), or they are difficult to exclude
because they become buried in the soil (Frazer et al. 1981a, Elvin et al.
1983). Cages also alter the
microclimate through shading and inhibiting air flow. Exclusion and partial exclusion cages
using terylene netting reduced the light intensity inside cages by 24-37%
(Campbell 1978) and saran screen reduced solar radiation by 19% (Hand &
Keaster 1967). Such shading required
the use of a more shade tolerant cotton cultivar than was normally planted in
the region (van den Bosch et al. 1969).
Shading also affects plant physiology and thus may affect the plant's
quality as a substrate for the host or prey population (Scriber & Slansky
1981). Temperatures within cages used
in a corn borer study were 8-10°F lower than the temperature outside. The humidity fluctuated more moderately
within and was 5-10% higher than that outside the exclusion cages (Sparks et
al. 1966).
11. Solar radiation changes
cause differences in leaf temperature by as much as 13°C (Hand
& Keaster 1967). Leaf
temperatures and moisture availability influence photosynthetic rates and
evapotranspiration (Gates 1980). Leaf
temperatures probably affect the behavior and feeding rates of phytophagous
hosts and prey. Temperature related
interactions between the growth rates of aphids and the searching rates of
their predators are important (Frazer & Gilbert 1976, Frazer et al.
1981a). Screening also reduced wind
speed within a cage by as much as 48% (Hand & Keaster 1967) which,
depending on RH and wind velocity outside and inside a cage, influences the
leaf's boundary layer within the cage (Gates 1980, Ferro & Southwick
1984). Instrumentation allows the
monitoring of many of these effects but their influence on predator/prey
interactions must be assessed (Luck et al. 1999). C. Removal by Insecticide
Treatment.
1. Natural enemy complex
impact may be assessed through the application of insecticides. The method was first used to kill natural
enemies of the long-tailed mealybug, Pseudococcus
longispinus (Targ.), without
affecting the mealybugs (DeBach 1946).
Insecticides have been used to determine whether indigenous predator
populations in cotton suppress populations of the beet armyworm, Spodoptera exigua (Hübner), and cabbage looper, Trichoplusia ni
(Ehler et al. 1973, Eveleens et al. 1973).
Early season insecticides applied to cotton were thought to interfere
with natural controls (Ehler et al. 1973, Eveleens et al. 1973). Large blocks (3-4 square miles) were
treated with an insecticide scheduled during early season, early and
midseason and early, mid- and late season.
A fourth plot served as an unsprayed control. Samples and observations showed that the
absence of predators in the treated plots was correlated with the increased
survival of beet armyworm eggs and first generation small larvae of the
cabbage looper. The hemipteran
predators, Geocorus pallens Stal, Orius tristicolor (White) and Nabis americoferus
Carayon were implicated as the most important predators since they were the
most affected by the treatments whereas Chrysoperla
carnea Stephen was not so
strongly affected. Insecticide
treatment showed that the suppression of cabbage looper densities in celery
arising from egg parasitism by Trichogramma
spp. and predation of eggs and young larvae by Hypodamia convergens
Guer. and O. tristicolor was sufficient to
prevent economic damage before the production of the first marketable petiole
in celery (Jones 1982).
2. Insecticides were also used
to test whether the coccinellid, Stethorus
sp. regulated the density of the two spotted spider mite, Tetranychus urticae (Koch), in a previously
untreated apple orchard in Australia (Readshaw 1973). Two applications of malathion increased
the density of the mite populations. Tetranychus urticae, unlike the predator
fauna associated with it, was resistant to malathion. Stethorus
regulated the mite population by numerically responding both aggregatively
and reproductively to the denser mite patches. Even with insecticide disruption and stimulation of the mite
reproduction (Chaboussou 1965, Bartlett 1968, van de Vrie et al. 1972, Dittrich
et al. 1974), Stethorus was
able to prevent the mite population from attaining an economic density of 100
mites/leaf on most trees.
3. The action of two
parasitoids of the olive scale, Parlatoria
oleae (Colvee), was
evaluated using insecticides (Huffaker & Kennett 1966). This scale is bivoltine on olive in the
San Joaquin Valley of Calviornia. One
generation occurs during the autumn and spring and the second generation
during summer. Aphytis paramaculicornus
DeBach & Rosen and Coccophagoides
utilis Doutt was introduced for
biological control (Rosen & DeBach 1978). Aphytis
dominated during the autumn and spring scale generation whereas Coccophagoides dominated during
summer. Three DDT treatments were
used to exclude the parasitoids: (1) a spring treatment to exclude Aphytis, (2) as summer
treatment to exclude Coccophagoides
and (3) a spring and summer treatment to exclude both parasitoids. Untreated trees were left as
controls. It was thought that DDT
residues on the foliage and twigs inhibited the parasitoids but did not
affect the scale's reproduction and survival. Treatments which excluded Coccophagoides
had higher scale densities than the untreated controls but lower densities
than the treatments which excluded Aphytis. Treatments that excluded only one of the
parasitoids had lower scale densities than treatments that excluded both
parasitoids. Treatments also
indicated that together the parasitoids provided better biological control
than either did alone even though the mortality contributed by Coccophagoides was only about
5%.
4. Inoculation of fumigated
(12 hrs with methyl bromide) and unfumigated poultry manure with Musca
domestica L. eggs
demonstrated 53.4 to 99.4% mortality in the presence of predatory and
scavenger arthropods (Legner 1971).
Significant negative correlations of parasitization with increasing
host densities were explained by parasitoid behavior. Inherently, single female parasitoids
without interference from other individuals of the same or different species
respond positively with increases in host density; parasitization rates
increase, which appears to be correlated with increases in the production of
progeny (Legner 1967). However, when
groups of parasitoids concentrate their search among several host pupae, as
is common in nature, their efficiency per female is decreased through mutual
interference, that apparently involves combinations of physical interruption
and chemical effects. There was some
evidence that female parasitoids were strongly attracted to denser
concentrations of their hosts in their habitat (e.g., Legner 1969), which
evidence further tends toward increases in the interference factor at natural
high host densities. Furthermore, any
interference that would deter some female parasitoids from oviposition during
the first few days of adult life would lower fecundity and longevity (Legner
& Gerling 1967). Operating
collectively, these several forces would tend to produce the observed
apparent negative correlation between parasitization and host density.
5. Several problems are
associated with interpreting results from an insecticide treatment,
however. The pesticide may stimulate
reproduction of the prey population.
There may be a pesticide induced sex ratio bias, and pesticide induced
physiological effects on the plant may arise. Mites that are exposed to sublethal doses of some pesticides
are stimulated reproductively and occasionally even increase female biased
sex ratios (Charboussou 1965, Bartlett 1968, van de Vrie et al. 1972,
Dittrich et al. 1974, Maggi & Leigh 1983, Jones & Parrella
1984). Such effects may also extend
to aphids (Bartlett 1968, Mueke et al. 1978), and delphacids (Chelliah et al.
1980, Reissig et al. 1982).
Differential mortality resulting from pesticide treatments has also
been reported. Male black pineleaf
scale, Nucalaspis californica (Coleman) (Edmunds
& Alstad 1985), and California red scale, Aonidiella aurantii
(Maskell) (Shaw et al. 1973) are more susceptible to pesticides than
females. Plant physiology is also
affected by insecticide applications (Kinzer et al. 1977, Jones et al.
1983). Row crops treated with certain
insecticides become attractive oviposition sites for Lepidoptera (Kinzer et
al. 1977). Interactions between aphid
reproduction, insecticides and cultivars have been reported on alfalfa (Mueke
et al. 1978). Knowledge of the
biology and interactions is required to properly time an insecticide
application to disrupt the natural enemy populations while minimizing their
effects on prey or host. Because
insecticides potentially stimulate arthropod reproduction and effect plant
physiology, estimates of predation rates with this exclusion method should be
done cautiously. Although insecticide
treatments stimulated the brown planthopper, Nilaparvata lugens
Stal, reproduction, the amount of stimulation could not account for the high
levels of resurgence. Only the
reduction of natural enemies could.
Insecticides can be used to determine the relative importance of
natural enemies when the complex is composed of a few species showing
temporal separation of their effects, in seasonal occurrence or in the
generations they attack (Luck et al. 1999). D. Removal of Natural
Enemies by Hand.
1. Although laborious, hand
removal has been used to evaluate the predators of tetranychid mites on
citrus and avocado and to compare results obtained with other exclusion
methods (Fleschner et al. 1955, Fleschner 1958). It has also been used to evaluate the mirid, Crytorhinus fulvus Knight, introduced to
control the taro leafhopper, Tarophagus
proserpina (Kirkaldy)
(Matsumoto & Nishida 1966).
Predation of Aphis fabae was also assessed in part
by removing adult predators by hand when they flew onto predator free
branches (Way & Banks 1968). A
sticky band at the base excluded walking predators from feeding on A. fabae individuals placed on the branch.
2. Luck et al. (1999) believe
that the hand removal method deserves more attention, especially as a method
of checking for bias in other exclusion methods. However, it seems to be limited to studies of predator/prey
interactions with species of low vagility, those that occur at reasonable
densities and are diurnally active or are undisturbed by night lights (Luck
et al. 1999). E. Prey Enhancement.
1. Prey may be placed directly
on plants in the field to stimulate predator attraction. This procedure involves tethering prey to
a substrate (Weseloh 1974, 1982) or placing them on leaves or other plant
parts where they would normally occur (Ryan & Medley 1970, Elvin et al.
1973, van Sickle & Weseloh 1974, Weseloh 1974, 1978, 1982; Torgensen
& Ryan 1981). Some studies marked
the prey with dyes before placing them in the field (Hawkes 1972, Elvin et
al. 1973). The prey were visited
frequently to measure predation, and if predation was observed, the
predator's identity was noted.
Predators such as spiders can be observed in the field with their prey
*Kiritani et al. 1972), and web spinning spiders leave cadavers in or beneath
their webs (Turnbull 1964). 2. It is sometimes more practical to use
greenhouse grown plants of the same age, size and variety as plants used in
field studies. Plants can be caged in
the greenhouse or field for pest oviposition. Then the infested plants are transferred to the field and
monitored for parasitism and predation.
Van der Berg et al. (1988) used eggs of several foliage-feeding rice
pests to determine predation. The egg
chorion showed that eggs were attacked by predators with chewing or sucking
mouthparts.
3. Predation and parasitism
was thought to alternate as principal mortality factors during the year in
studies that followed the seasonal incidence of predation and parasitism of
eggs of the yellow stemborer of rice, Scirpophaga
incertulas (Walker) (Shepard
& Arida 1986). The technique of
prey enhancement may be used to advantage with cages and or
insecticides. However, a major
limitation is that prey must be limited to sessile forms such as eggs, pupae
or some scale insects, although there are possibilities with tethered hosts
(Weseloh 1974). Kairomones and other
chemical cues may be important to establishing the appropriate interaction
(Nordlund et al. 1981). VII. Methods For
Detecting Predation/Parasitism A. Serology. 1. Predators have been associated with their
prey with serological methods (Dempster et al. 1959, Dempster 1960, 1964,
1967; Rothshild 1966, 1970, 1971; Frank 1967, Ashby 1974, Vickermann &
Sunderland 1975, Boreham & Ohiagu 1978, Sunderland & Sutton 1980,
Gardner et al. 1981, Greenstone 1983).
Predations rates have also been estimated with serology (Dempster et
al. 1959, Dempster 1960, 1964, 1967).
A precipitin assay has been also used (Boreham & Ohiagu 1978,
Ohiagu & Boreham 1978, Southwood 1978).
Other methods are the enzyme-linked immunosorbent assay (ELISA)
(Vickermann & Sunderland 1975, Fichter & Stephen 1979, 1981, 1984;
Ragsdale et al. 1981, Crook & Sunderland 1984, Sunderland et al. 1987,
Sopp & Sunderland 1989), and an assay based on passive hemagglutination
inhibition (PHI) (Greenstone 1977, 1979).
Agglutination assay employs polystyrene latex particles coated with
antibody (Boreham & Ohiagu 1978, Ohiagu & Boreham 1978). Such methods detect prey particles in the
gut of predators by its reaction with antibodies obtained from a vertebrate,
such as a rabbit, that has been sensitized to the prey. The reaction is a visible
precipitate. (Also see Boreham &
Ohiagu 1978, Miller 1978 and Sunderland 1988).
2. Detection of prey in a
predator's gut is influenced by the size of prey, size of meal, time since
the meal was taken, the rate of digestion, whether the natural enemy is a
sucking or chewing predator, the abundance of taxonomically closely related
prey and the sensitivity of the test.
Sensitivity of the assay can be increased if the antibody is linked to
an enzyme (ELISA). When the antibody
reacts with prey, the enzyme carried with the antibody allows amplification
of the reaction because one enzyme molecule can convert many molecules of
substrate. This assay may detect
hemolymph dilutions of more than 260,000 (Fichter & Stephen 1981) and is
often sufficient to differentiate among prey stages (Ragsdale et al. 1981). 3. Both precipitation and ELISA techniques
are useful for identifying the prey in a predator's diet and estimating
predation rates (Sunderland 1988).
ELISA is more sensitive to the presence of small amounts of antigen
(prey protein or carbohydrate), is suitable for large scale testing and can
be used with a minimum of equipment.
Material necessary for the tests may be prepared and stored under
refrigeration for six months (Sunderland 1988).
4. The passive
haemagglutination assay (PHA) is a method for increasing sensitivity of the
precipitin test. Sheep red blood
cells (rbc) are chemically coated with the antigen of the suspected
prey. Antigen coated rbc's are added
to a solution of specific antibody and combine with the antigen molecules on
the rbc to form a mat (agglutination).
Small amounts of antibody cause agglutination. In antibody-free controls the rbc's do not
agglutinate and this inhibition forms the basis of the assay. The amount of antibody required to cause
agglutination is determined and added to an extract of a predator's gut
contents. If prey protein or
carbohydrate (antigen) is present it binds with the antibody. When antigen coated rbc's are added, they
will not agglutinate because the antigen from the predator's gut has been
bound by the antibodies (Luck et al. 1999).
A small amount of antigen produces inhibition which explains the
assay's greater sensitivity than that of a comparable precipitin assay
(Greenstone 1979). Freshly sensitized
erythrocytes have to be prepared each time an assay is conducted (Boreham
& Ohiagu 1978), and this requires skilled operators. 5. The precipitin test was originally used to
document arthropod predation of mosquito larvae (Bull & King 1923, Hall
et al. 1953, Downe & West 1954) and latter was applied to terrestrial
predator/prey interactions (Downe & West 1954). The first prey for which estimates were attempted from field
samples was a chrysomelid beetle Gonioctena
(= Phytodecta) olivacea (Forster) feeding on
broom (Dempster 1960). Tests revealed
six mirids, two anthocorids, a nabid, a dermaptern and red mites feeding on
the beetle in the field. Laboratory
tests showed that only the older mirid and anthocorid stages fed exclusively
on younger stages of G. olivacea. A single laboratory feeding by the mirids
and anthocorids could be detected 24 hrs after they had ingested a meal, and
feeding by a dermapteran could be detected 60 hrs after it had fed (see Luck
et al. 1999). 6. The degree of overlap between older stages of the predator and younger
stages of the beetle influenced the number of beetles preyed upon. Densities of prey and predators were
estimated from field samples. The
fraction of positive responses in predator samples estimated the fraction of
the predator population that had fed on G.
olivacea. Because G. olivacea
were scarce in the field while alternative prey were abundant, encounters
between G. olivacea and the predators were
infrequent. Therefore, if a predator
tested positive to G. olivacea antibody, it was interpreted
as a single predation event. Then the
number of beetles preyed upon by each predator could be estimated suing the
equation: Pa =
(NpiFpiTpi) / Rpi where Pa is the number of prey killed; Npi
the density of the predator (or stage of predator) i; Fpi the
fraction of positive tests of the ith predator in a sample; Tpi
the duration in days that the appropriate prey and predator stages are
coincident in the field; and Rpi the retention time of a single
prey feeding by ith predator (or stage of predator). Estimates from the precipitin test of egg
and larval mortality due to predator for two beetle generations were found to
agree closely with the independent estimates of "unknown" losses of
eggs and young larvae during the same two beetle generations (Richards and
Waloff 1961).
7. The precipitin test also
was used to identify the predator species and to determine the fraction of Pieris rapae (L.) eggs and young larvae that died due to
predation (Dempster 1967). Because of
the relative scarcity of P. rapae a positive precipitin
test was interpreted as one predation event.
Studies of the delphacid Conomelus
anceps (Germar) employed
precipitin tests to identify ten of 91 potential predators (Rothchild 1966). The precipitin test could not be used to
estimate predation rates because multiple predation events were
possible. 8. For estimating predation rates with the
precipitin test it is necessary to have information about predator and prey
densities, densities of alternate prey, the period during which a meal can be
detected in each predator and prey and predator stages involved. Precipitin tests estimate predation rates
of prey which form a small fraction of the available prey or infrequent
predation events. A slight bias may
arise in such estimates if predators have fed on other predators that have
fed on the prey, if a suspected predator is phytophagous but ingests sessile
prey stages while feeding on the plant or if a suspected predator feeds on
prey carrion (Boreham & Ohiagu 1978).
The precipitin test may also yield biased estimates of predation rates
from cross reactions between the antibodies of closely related species. Therefore, a knowledge of the local fauna
which might serve as prey and the predator's propensity for local movement is
essential to the successful application of this test (Luck et al. 1999). Also the serum developed from one prey
stage may not react with the antigen of another (Boreham & Ohiagu
1978). Sufficient resources must be
committed in order to use this technique:
prey must be collected in sufficient numbers to elicit an
immunological response when injected into the vertebrate. As such the procedure is not ideal when
applied to small prey such as mites (Murray & Solomon 1978). 9. When used in conjunction with other population studies,
precipitin assays may be very helpful.
Few other methods can provide quantitative estimates of predation
rates under natural field conditions.
Although they cannot be used to estimate predation rates under all
situations, they are valuable for identifying predator species or stages that
feed on a prey. This method deserves
more attention especially as more sensitive tests such as ELISA are available
(Vickermann & Sunderland 1975, Fichter & Stephen 1981, 1984; Ragsdale
et al. 1981, Crook & Sunderland 1984, Sunderland et al. 1987, Soop &
Sunderland 1989). A great advantage
is that predation is allowed to occur naturally. B. Electrophoresis
& Isoelectric Focusing. 1. Predators may be associated with the prey with electrophoretic
techniques. Electrophoresis separates
proteins based on charge and size differences in an electrical field. Differences in charge and size commonly
occur among isoenzymes (proteins catalyzing the same reaction) from different
taxa. If the prey and predator have
isoenzymes with different electrophoretic mobilities, the analysis of
homogenates prepared from predators fed on prey should exhibit protein bands
corresponding to the predator and the prey.
Also if there are several potential prey of a predator, and if the
prey have electrophoretically distinct isoenzymes, analysis of predator
homogenates can reveal the prey species inside the predator. 2. Electrophoresis can be successful if the prey isoenzymes are
detectable after predator feeding, and electrophoretic variation occurs among
the prey and predator isoenzymes.
Isoenzyme detection depends on prey size, in vitro
activity of the isoenzyme, presence and volume of the predator foregut, and
the type of electrophoresis employed (Murray & Solomon 1978, Giller 1984,
Lister et al. 1987, Soop & Sunderland 1989). Electrophoretic variation depends on the suite of isoenzymes
available for comparison and the type of electrophoresis. Standard electrophoretic procedures
(starch gel and polyacrylamide gel electrophoresis) can detect prey isoenzyme
activity for several isoenzyme types involving relatively large prey (>2-3
mm body length). Under this size, the
number of detectable prey isoenzymes is diminished and hence the chance of
distinguishing closely related prey is decreased. 3. Enhanced sensitivity of electrophoretic
methods include conventional electrophoresis in cellulose acetate membranes
(Easteal & Boussy 1987, Höller & Braune 1988) and isoelectric
focusing (IEF) (see Luck et al. 1999).
IEF has advantages over other techniques involving small and large
prey. In IEF, proteins are
"focused" into narrow bands along relatively broad pH
gradients. Focusing enhances the
detection of enzymes compared to other techniques which gradually spread the
proteins into diffuse bands. In
addition, because relatively broad pH gradients are used in IEF, enzymes with
different charges, such as may occur between unrelated prey taxa, will remain
sharply focused on the gel. The fine
resolution of IEF does not affect the ability to distinguish enzymes with
very similar charges. With standard
techniques, these contrasting problems are difficult to solve simultaneously
as one set of conditions (buffer type and pH, gel type) may be optimal for
one prey type but not others. 4. The prey of several arthropod predators
have identified with electrophoresis.
Polyacrylamide gradient gel electrophoresis was used to detect prey
protein (esterases) in the gut of predators after they had fed on known prey
(Murray & Solomon 1978). The technique
detected esterases of Panonychus
ulmi (Koch) in the
predaceous mite Typhlodromus
pyri (Scheuten), and in two
anthocorids, Anthocoris nemoralis (F.) and Orius minutus (L.) that had fed on the mite in the
laboratory. Dicke & DeJong (1986)
used methods to determine whether T.
pyri and Amblyseius finlandicus (Oudemans) also fed on the apple rust mite, Aculus schlechtendali (Nalepa) as an alternate host in the
field. Electrophoresis was also used
to identify the prey species exploited by A.
nemoralis on alders in the
field (an aphid Pterocallis alni [DeGeer]) (Murray &
Solomon 1978). Electrophoresis with
polyacrylamide disc gels detected esterases of several prey species in the
gut of the waterboatman Notonecta
glauca L. (Giller 1982,
1984, 1986). A meal was detectable
from 17-48 hrs depending on temperature and meal size, and was strongly
correlated with the length of time the meal spent in the foregut (Giller
1984). Giller (1986) used
electrophoresis to identify the prey of N.
glauca and N. viridis Delcourt in the field. Lister et al. (1987) used polyacrylamide gel electrophoresis
and electrophoresis and esterase allozymes to determine the diet of some
microarthropods and the predation rate by the acarine predator Gamasellus racovitzai (Trousessart).
5. Predation rate estimates
with serological methods and electrophoresis requires substantial
resources. The techniques call for
the development of antibodies or methods for identifying the isozymes of the
prey species or stage, the development of methods to estimate the predator
and prey densities, including those needed to estimate the densities of
alternate prey, and the identification of the predator and prey stages
involved. Initially the use of these
techniques to estimate predation rates appeared limited to prey populations
which form a small fraction of the available prey or in which predation
events by a predator are frequent.
Frequent predation confounds interpretation of a positive test because
a single large meal cannot be distinguished from several small meals. 6.
Immature parasitoids within aphids have been detected with
electrophoresis (Wool et al. 1978, Castanera et al. 1983), and in whiteflies
(Wool et al. 1984). The parasitoid Aphidius matricariae Hal. was detected in the green peach aphid Myzus persicae (Sulz) and parasitism of the white fly, Bermesia tabaci (Gennadius) by the endoparasitoids Encarsia lutea (Masi) and Eretmocerus
mundus (Mercet), was
detected with electrophoresis and histochemical staining for esterases. But the whitefly parasitoids could not be
identified to species (Wool et al. 1984).
Electrophoresis allows the processing of large numbers of hosts to
estimate the fraction that are parasitized and sometimes the parasitoid
species involved. This contrasts with
the traditional methods in which field samples are dissected while fresh or
reared. Electrophoresis can detect
within a host immature parasitoids without dissection and parasitoid enzyme
activity within a prey cannot be confused with host's enzyme activity. C. Marking Prey. 1.
Predator species and/or predation rates have been identified with
marking techniques. Markers have
included radioactive isotopes -151europium (Ito et al. 1972), 32phosphorus
(Jenkins & Hassett 1950, Pendleton & Grundmann 1954, Jenking 1963,
McDaniel & Sterling 1979, McCarty et al. 1980, Elvin et al. 1983) and 137cesium
(Moulder & Reichle 1972), 14carbon (Frank 1967), rare elements
(Stimmann 1974, Shepard & Waddill 1976), and dyes (Hawks 1972, Elvin et
al. 1983). Prey are fed (Elvin et al.
1983, Frank 1967, Room 1987) or injected (McDaniel & Sterling 1979,
McCarty et al. 1980) with the radioactive isotope and the radioactivity is
detected in a predator with scintillation, a Geiger counter, or autoradiography. For autoradiography suspected predators
are collected after exposure to labelled prey and are glued to paper, which
is placed against X-ray film (McDaniel & Sterling 1979). The film is developed, and dark spots on
the film produced by the rays from 32phosphorus indicate labelled
predators. Methods involving isotopes
require training and necessary equipment to perform the assays. Safety regulations and environmental
considerations may limit the use of the method in some situations. Other disadvantages, as with
electrophoresis and serological techniques, include the inability to detect
whether a predator had fed on other predators that had consumed labelled prey
or whether a prey was scavenged (Luck et al. 1999). Experiments using isotopes, especially those using
autoradiography, are simpler to conduct than serological and related
techniques. Methods using labelled
elements require several manipulations, but they provide more information per
unit effort than other kinds of marker tests. 2.
Such rare elements as rubidium and strontium also have application as
labels. They can be sprayed on
foliage or placed in the diet of the prey, incorporated into the prey's
tissues and then transferred to the predators or parasitoids who feed on
labelled hosts (Stimmann 1974, Shepard & Waddill 1976). The mark should be retained for life, and
self-marking is possible via a labelled plant. However, the technique requires an atomic absorption
spectrophotometer, which is expensive, and placement of the labelled prey on
plants may expose them to abnormal predation rates. Phytophages seldom choose feeding or oviposition sites on their
plant hosts at random (Ives 1978, Wolfson 1980, Denno & McClure 1983,
Guerin & Stadler 1984, Whitham et al. 1984, Myers 1985, Papaj &
Rausher 1987). Parasitoids and
predators do not search their habitats uniformly (Weseloh 1974, 1982;
Fleschner 1950). Therefore, without
the proper behavior studies, the degree of bias in determining the natural
enemy complex or in estimating predation rates is unknown. 3. Genetic markers have been used to track
parasitoids and assess their impact against hosts, such as common muscoid
flies. Legner & Brydon (1966)
liberated a thelytokous race of parasitoid on poultry farms which they were
able to tract and derive host mortality data from. Legner et al. (1990, 1991) derived similar information by
releasing gregarious strains of Muscidifurax
raptorellus Kogan &
Legner, and a temporary interference of several weeks with resident
parasitism during the establishment phase was detected. However, this was later overcome when the
released strain had a chance to multiply naturally at the site. D. Visual
Counts.
1. There are several
advantages of using visual counts over many of the exclusion techniques. There is no manipulation of the
environment required. Prey can be
added or predators removed to determine the response of the predator to
changes in prey density. A visual
record reveals the predator's diet in the field. Perhaps serology and electrophoresis share these three
advantages, but the latter require considerable technology. visual counts require a substantial
commitment of time to observe the predation and to determine the feeding
rates for different combinations of predator/prey stages.
2. Vision cannot be used if
the predator is cryptic, easily disturbed or escapes from the observer. Also, the time a predators spends
consuming a prey may vary depending on the range of prey stages attacked, the
hunger level of the predator, interference or stimulation by other predators
or prey that are active in the area, and differences among individual
predators due to genera, reproductive stage or molting (Luck et al.
1999). These in turn can determine
the probability that a predator will be observed in the field with a
prey. Laboratory data on the time
spent by four predators consuming prey was highly variable, leaving the
investigators pessimistic about the visual method's utility for estimating
predation rates (Kiritani et al. 1972).
But the approach may still be valid for some predators, and has been
used to determine the fraction of diurnal predation for each predator species
in a complex (Elvin et al. 1983). E. Statistical Sampling. 1. Obtaining field samples during
parasitoid/predator liberation periods can provide useful information about
the ability of a species to effect its host/prey density. Parasitoid impact was thus measured on the
pink bollworm, Pectinophora gossypiella (Saunders). A significant positive relationship was
found between the total number of parasitoids released and the host density,
which was most pronounced during a mid autumn period (Legner & Medved
1979). Releases of egg-larval and
larval-parasitoids produced small measurable reductions in P. gossypiella moth emergence from mature cotton bolls, but
did not significantly reduce % boll infestation. By releasing parasitoids at three densities, it was possible to
show significant differences between controls and a low and medium release
rate, but excessive parasitoid dispersal out of the release areas into the
cotton field at large explained a leveled slope after the medium release rate
(Legner & Medved 1979).
2. The potential of Goniozus spp. and Pentalitomastix plethorica Caltagirone to
regulate navel orangeworm, Amyelois
transitella (Walker) was
judged from seasonal positive functional responses to host density and with
k-value analyses (Varley et al. 1974, Legner & Silveira-Guido 1983). Application of this technique requires
that the host show minimal overlapping of generations, however. Goniozus
emigratus (Rohwer) and Goniozus legneri Gordh demonstrated a significant capacity to
recognize and respond in a regulative fashion in mid summer by increasing
attack rates on higher host densities.
However, no such tendency was indicated during cooler periods of late
autumn. 3. Indigenous parasitism of Rhagoletis completa Cresson in its native range of western Texas and
southeastern New Mexico was also assessed with k-value analysis,which showed
a significant impact of combined natural mortality on host reduction (Legner
& Goeden 1987). Biosteres sublaevis Wharton demonstrated the greatest measurable
activity as a cause of natural mortality.
4. Legner & Brydon (1966)
were able to show an increased parasitism and house fly host mortality closer
to liberation sites of parasitoids.
Legner et al. (1990, 1991) also charted increases and spread of
muscoid fly parasitism from release sites.
The importance of proper field sampling, measurement of host
destruction and unpredicted upsets to organisms in different guilds in these
and similar studies was emphasized (Legner & Bay 1964, Legner 1979,
Legner 1983, 1986). 5. Long
term sampling of the width of aquatic weed masses following the introduction
of phytophagous cichlid fish established a regulatory capacity for Tilapia zillii Gervais in California irrigation canals (Legner
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