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OCR for page 165
14
Biological Control of
California Red Scale
interest in biological control of agricultural pests has been stimulated
by the evolution of resistance of the target organisms to pesticides, by
secondary outbreaks caused by losses of natural predators and parasites,
and by the increasing seriousness of unwanted side effects of pesticides
on many species, including humans. However, biological control is not
yet a highly predictive branch of ecology. Most biological control efforts
fail, either because the control agent does not survive or because, if it
survives, it does not result in satisfactory control. The California red scale
study illustrates features common to many instances of biological control,
but it also shows how imaginative use of some new elements of ecological
theory, such as those related to foraging and sex allocation, led to changes
in project organization that illuminated the processes underlying effective
biological control.
165
OCR for page 166
Case Study
ROBERT F. LUCK, Department of Entomology, University of California,
Riverside
INTRODUCTION
California red scale, Aonidiella aurantii (Maskell) (Diaspididae:
Homoptera), is an insect pest of citrus in arid and semiarid regions
(Bodenheimer, 1951; Ebeling, 19591. It inhabits all aboveground parts
of a citrus plant. At moderate densities, the scale infests the fruit, which
might then be culled in accordance with industry standards for ap-
pearance. At higher densities, it inhibits fruit production and kills
branches. In California, it is one of three principal arthropod pests of
citrus and infests all four major cultivars grown in the state: grapefruit,
lemons, and two orange varieties.
California red scale was introduced into southern California between
1868 and 1875 on shipments of citrus nursery stock from Australia
(Quayle, 19381. Lindorus lophanthae (Blaisd.) (Coccinellidae: Co-
leoptera), a predatory ladybird beetle introduced from Australia, was
the first of 52 predators and parasites (36 and 16, respectively) intro-
duced against California red scale. Of the eight that became established,
three were predators L. Iophanthae, introduced in 1889; Orcus cha-
lybeus (Bvdl.), in 1892; and Chilocorus similis, in 1924- 1925 and
five were parasitoids Comperiella bifasciata Howard, in 1940; Ha-
brolepis rouxi Compere, in 1937-1939; Aphytis lingnanensis Compere,
in 1948; Encarsia (= Prospaltella) perniciosi Tower, in 1949; and A.
melinus DeBach, in 1956-1957 (Rosen and DeBach, 19781. Aphytis
chrysomphali (Mercet), a thelytokous (parthenogenetic, mostly female-
producing) parasitoid, was unknowingly introduced around 1900, prob-
ably in parasitized scale on infested nursery stock from the Mediter-
ranean Basin (Rosen and DeBach, 1978, 19791.
Before the introduction of the wasp Aphyt~s lingnanensis (Aphelinidae:
Hymenoptera), in 1947, California red scale was economically controlled
by A. chrysomphali in the Santa Barbara, California, area (DeBach and
Sisojevic, 1960), perhaps with some help from ladybird beetles, so long
as ants, dust, and insecticide interference were minimized. The scale
remained a problem, however, in inland coastal valleys and other coastal
areas, even though A. chrysomphali was found throughout these regions.
When A. Iingnanensis was introduced, biological control was achieved in
166
OCR for page 167
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
167
most coastal areas. But only with the introduction of A. melinus in 1956-
1957 was biological control achieved in inland valleys (Rosen and DeBach,
1979~.
In contrast with the situation in southern California, economical bio-
logical control of California red scale does not exist in the San Joaquin
Valley or the desert, even though both Comperiella bifasciata (Encyrtidae:
Hymenoptera) and A. melinus are present. Remaining natural enemy spe-
cies, both introduced and native, are scarce. Moreover, citrus production
in the San Joaquin Valley is assuming increasing importance as that in
southern California declines with increasing urbanization. In the absence
of economic biological control of scale, growers have relied on synthetic
organic insecticides (Flaherty et al., 19731.
THE ENVIRONMENTAL PROBLEM
Synthetic organic insecticides have several drawbacks. Their initial
effectiveness, convenience, and low cost all promote their use (Luck et
al., 19774. But these materials are general in their effects, so they also
kill native predators and parasites of the target pests, as well as the pests
themselves, and sometimes cause outbreaks of the target pests and sec-
ondary pests (phytophagous arthropods normally held at bay by their
natural enemies3. Pesticide applications increase the nutritional value of
plants for some prey species (Dittrich et al., 1974; Jones and Parrella,
1984; Maggi and Leigh, 19831. Pest resurgence and secondary-pest out-
breaks promote further pesticide use, and the grower becomes enmeshed
in a pesticide treadmill in which still further pesticide use increases control
costs and selects for resistance in primary or secondary pest species (Luck
et al., 19771.
Citrus is one of many crops that have followed this scenario (Luck et
ale 19771. California red scale populations in South Africa, Israel, and
Lebanon have evolved resistance to one or more of the synthetic organic
scalicides (Georghiou and Taylor, 19771. California populations have evolved
resistance to hydrogen cyanide gas, used as a fumigant before World War
II. Secondary-pest outbreaks have also occurred in citrus. Since the 1960s,
several Lepidoptera species and citrus red mite, Panonychus citri McG.
(Tetranichidae), have become increasingly frequent pests in California
citrus because of insecticide use (Luck et al., 19771. Citrus red mite has
also evolved resistance to many acaricides used against it (Georghiou and
Taylor, 19774.
OCR for page 168
168
SELECTED CASE STUDIES
ECOLOGICAL APPROACH TO THE
ENVIRONMENTAL PROBLEM
We have had two objectives in our studies of California red scale, its
host plants, and its natural enemies: the specific objective of improving
the biological control of the scale, especially in the San Joaquin Valley,
and the general objective of understanding how biological control of red
scale works and what limits its success. The latter objective presupposes
that understanding the reasons for success and failure and the associated
processes and mechanisms in a specific case will improve our ability to
predict the outcome both of this particular natural enemy-pest interaction
and of such interactions in general.
The specific objective motivates a continuing biological control project,
whose key components are the obtaining and manipulation of natural
enemies of the scale, the importation of exotic predator and parasitoid
species reared from California red scale or related species around the
world, and the mass rearing and release of endemic and exotic natural
enemies. We seek by these means to develop practical and economical
ways of augmenting endemic natural enemy populations by releasing in-
sectary-reared individuals. The duration of this project depends on the
discovery of new species of natural enemies, on political conditions in
the geographical region where we wish to collect natural enemies, and on
the degree of biological control achieved by introducing enemies. Im-
portation and release of natural enemies would cease once effective bio-
logical control were achieved throughout California.
We have pursued the general objective of using California red scale as
a model system through a combination of field and laboratory studies to
identify attributes and processes that characterize a successful biological
control project. Laboratory studies have sought to understand the host
selection and foraging behavior of the several natural enemies of California
red scale. The results suggested hypotheses to be tested with field pop-
ulations of the scale. In addition to field tests of hypotheses (e.g., aug-
mentative releases), comparative demographic studies of red scale
populations were begun in three of California's four citrus regions; these
studies sought to evaluate the effect of natural enemies on the dynamics
of red scale populations (cf. Rosen and DeBach, 1978) and to provide a
baseline for assessing new introductions.
OCR for page 169
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
USES OF KNOWLEDGE AND UNDERSTANDING
Ecosystem Definition
169
The ecosystem components of interest in these studies are several citrus
cultivars grown in commercial and dooryard plantings in the state, hon-
eydew-producing insects and ant species that tend them, natural enemies
that attack California red scale and its primary natural enemies, California
red scale, and climates in the three citrus regions. Also of interest are
associated phytophagous arthropods that receive frequent or occasional
insecticide treatments, whose consequences can affect red scale or its
interaction with its natural enemies. Chemical control of red scale might
also affect densities of other phytophagous species or their natural enemies,
including the citrus thrips, Scirtothrips citri (Thripidae: Thysanoptera),
citrus red mite, and several lepidopterans (Luck, 19841. With increasing
information and understanding, we might also need to include other com-
ponents of the ecosystem, such as citrus nematode, phytophthora root rot,
or Tristeza (seedling yellows), because they and their treatment influence
the physiology of the tree or otherwise affect the interaction between red
scale and its entomophages. The ecosystem components named earlier
were identified because they were economically important or because
previous research with citrus, with other agricultural ecosystems, or with
natural ecosystems suggested that these components were biologically
important.
Significance of impact
If biological control of California red scale is achieved, chemical control
will be required only infrequently when weather patterns, dust, insecticides
(drifting from adjacent crops from treatments of an associated pest), or
ants interfere with the scale's natural enemies and thus induce increases
in local scale populations. Biological control should reduce red scale
population densities, pest-control costs, and pesticide-related environ-
mental and health problems. These expectations are based on experience
with biological control of pests in general and of red scale in both southern
California (Rosen and DeBach, 1978, 1979) and other citrus-growing
regions, such as Greece (DeBach and Argyriou, 1967), Australia (Furness
et al., 1983), South Africa (Bedford and Georgala, 1978), and Cyprus
(Orphanides, 19841.
OCR for page 170
170
SELECTED CASE STUDIES
Study Strategy and Monitoring
Our first specific goal associated with the second objective was to
understand why Aphytis melinus replaced a. Iingnanensis in southern
California and what limits the degree of parasitism achieved by A. Iing-
nanensis. A. Iingnanensis was first introduced into California in 1947. It
was not the first Aphytis present on red scale in California, however; A.
chrysomphali had apparently been introduced before 1900 (Rosen and
DeBach, 19791. A. Iingnanensis replaced A. chrysomphali, probably be-
cause it was better adapted to the climate of California's citrus districts
(DeBach and Sisojevic, 19601. However, A. Iingnanensis failed to achieve
economic scale control in the more interior citrus districts, so additional
natural enemies were sought. One of these, A. melinus, was established
in the interior in 1956-1957 and quickly spread throughout the area, dis-
placing A. Iingnanensis. A melinus provided economic scale control in
much of southern California. In the late 1970s, the three species were
distributed as follows: A. melinus in the interior citrus areas, A. Iingna-
nensis along the coast and inland approximately 10 km, and A. chrysom-
phali as a relict in a few coastal enclaves (loosen and DeBach, 1979~.
DeBach and his co-workers monitored establishment and spread of these
introduced Aphytis species by sampling red scale populations in many
places throughout southern California (DeBach, 19651. DeBach noticed
A. melinus displacing A. Iingnanensis. In some groves, the displacement
occurred even when third-stage female scale, the putative host for the two
Aphytis species, was abundant. DeBach concluded that hosts for the par-
asitoids were not limiting and that competition for scarce hosts could not
explain the displacement (DeBach, 1966; DeBach and Sundby, 1963;
Rosen and DeBach, 1979~. Laboratory experiments designed to test this
hypothesis, however, contradicted the field observation: A. Iingnanensis
displaced A. melinus in the laboratory-the opposite of what happened
in the field (DeBach and Sundby, 19631. DeBach then suggested that A.
melinus performed better in the field because it was both a better searcher
and better adapted to California's climate than A. Iingnanensis.
Established Boundaries
For demographic studies, we used the citrus tree as a sampling universe.
Such a universe is reasonable for characterizing an interaction between
red scale and its natural enemies because red scale is mobile only during
the crawler stage (first instar) and, in the case of male scale, briefly (less
than 24 hours) as an adult while seeking mates. Between-tree movement
depends on wind dispersal of crawlers and sometimes on crawlers that
OCR for page 171
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
) I As (HICO N
~\`,) ~ ~
\ · \ O 50 100 MIL E S
\ SACRAMENTO ~
SAN ~\
FRANCISCO \4 ,__` \
~ '' \\ \
ESNO \
\ \
~ _ ~
SAN LUIS OBISPO).
SANTA BARBARA
`/rKeT. .~.~ ~
.~.'PORTERVILLE \
~ \ \
\
BAKERSFIELD
V 1~1~ 1 -1~0-~- Cal \ - - -
LOS ANGELES. ~ ~
'it
SAN DIES
FIGURE 1 Climatic zones in which California citrus is grown.
171
wale between contiguous trees. Adult natural enemies can easily fly be-
tween trees, but we understand little of their behavior or patterns of
movement. However, because we wanted to know the effects of natural
enemies on the red scale population of a tree, it seemed reasonable, at
least initially, to consider the natural enemies on a within-tree basis also.
For our studies of economic effects, we again used the tree as a universe,
but we were also concerned with the economic effects of biological control.
Thus, we chose "blocks" (management units of citrus groves) of about
2.5 hectares as our economic universe.
We limited our study to California citrus groves and dooryard citrus.
We divided the state's citrus growing areas into zones (Figure 1) on the
basis of climate and industry experience. We used the differences between
zones as manipulations with which to compare changes in the scale's age
structure caused by seasonal temperature patterns and the influence of
these changes on control of the scale.
Developing and lmpiementing a Study Strategy
We first tested DeBach's assertion that A. melinus and A. Iingnanensis
used the same host resource (scale stage and size) (DeBach, 1966; DeBach
OCR for page 172
172
SELECTED CASE STUDIES
and Sundby, 1963; Rosen and DeBach, 1979) by characterizing the ovi-
position behaviors of the two species. We used these behaviors to see
what the parasitoids recognized as hosts and how many eggs of what
gender they chose to allocate to those hosts (male, female, or mixed
gender). An Aphytis egg is laid on the host's body beneath a scale cover
where it cannot be seen, but the laying of an egg is reflected in obvious
oviposition behavior (Luck et al., 1982) (Figure 21.
We next determined what size and stage of scale each wasp species
used as hosts for its progeny. Most hymenopterans, including A. melinus
and A. Iingnanensis, have diploid females and haploid males. Thus, the
parental female determines the gender of her offspring by "deciding"
whether or not to fertilize the egg. Some hymenopterans lay male eggs
on small hosts and female eggs on large hosts (Charnov, 1982; Charnov
et al., 198 1; Chewyreuv, 1913; Clausen, 19391. This behavior charac-
terizes both A. melinus (Figure 3) and A. Iingnanensis (Figure 4), although
A. melinus allocates sons and daughters to smaller scale than does A.
Iingnanensis (Luck and Podoler, 19851. We hypothesized that A. melinus
displaced A. Iingnanensis because it usurped a substantial proportion of
the scale population before scale attained the size that A. Iingnanensis
required for its offspring especially the size needed to produce daughters.
Both Aphytis species paralyze the scale before they deposit eggs on it,
thus preventing further scale growth. As a scale grows, it attains the size
used by A. melinus first. Use of the scale by A. melinus then eliminates
the scale as a potential resource for A. Iingnanensis. Each species tends
to avoid depositing eggs on scale previously parasitized by the other (Luck
and Podoler, 19851. Thus, the initial laboratory studies on host selection
by Aphytis led us to propose a hypothesis to explain how A. melinus
displaced A. Iingnanensis in southern California. Some of the predictions
derived from this hypothesis were testable in the field.
Specif c Predictions and Hypotheses
If our hypothesis is correct, A. melinus should eventually eliminate A.
Iingnanensis from southern California. Rosen and DeBach (1979) found
that in 1965 A. melinus occurred in the interior coastal valleys and that
A. Iingnanensis occurred along the coast to a point about 10 km inland.
By 1972, A. melinus had spread coastally while the area populated by A.
Iingnanensis had contracted (Luck and Podoler, 19851. In 1983, A. Iing-
nanensis was restricted to a few locations, all within a kilometer or so of
the coast (R. F. Luck and S. Warner, unpublished data).
The age structure of California red scale varies seasonally with location
in California. Lower winter temperatures inhibit crawler production by
OCR for page 173
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
HOST SEARCHING
HOST CONTACT
ANTE NN AT ION
~ \
HOST MOU N T I NG \
DRUMM I NG AND
TU RN I NG
DRILL ING
INSERTION OF OVIPOSITOR
INTO SCALE BODY
pi
R ~,
E
E
N
1
N
G
REJECTION Of-
-SCALE
i WITHDRAWAL I WITHDRAWAL I
OVIPOSITOR PROBING
INSIDE SCaLE BODY ~ HOST
FE EDI NG
I NSE RT ION OF OV' POS I, OR INSE PT ION Of OV! PO S ~ TO R
BETWEEN VENTRAL BETWEEN DORSAL
SURFACE OF SCALE SURFACE OF SCALE
BODY AND SUBSTRATE BODY AND SCALE COVE R
WITHDRAWAL MOVE MENT OF OVIPOSITOR
OF OVI POSITOR I
. .
ISt PUMPIN( , MOVE BENT
173
REMAINS | LEAVES
ON SCALE BRIEF REST SCALE
COVER COVE R
2nd PUMPIN G MOVENIE'JT
AND EGG DEPOSITION
WIT HDRAWAL-
FIGURE 2 Behavioral sequence exhibited by Aphytis melinus and A. Iingnanensis
during oviposition.
OCR for page 174
174
SELECTED CASE STUDIES
Ap~yt i s me l i nus
5 r HOST SIZES YIELDING 25! AND Ad, n.3
| 3 EGGS / HOST
(iSt,38' (a)
. .
~.3 .4 .5 .6 .7 .8 .9 1 0
S ~HOST SIZES YIELDING A; ANDES
n ~ 23 23i, 23 d'
2 EGGS / HOST I I I ~
4 .5 .6 7 8 .9 1 .0
(b)
12 13
5 HOST SIZES YIELDING At n= 24 24
I EGG / HOST
O I I I I I (C)
.3 4 .5 .6 7 .8 91 0 1 1 1.2 1 3
5 ~ HOST SIZES YIELDING A]
I EGG / HOST
0' ~ · ~
3 .4 5 6 7 8 9 1.0 1 1 1.2
n= 6 6d.
(d)
~,.
1 3
5
Z HOST SIZES PARASITIZED n = 121
i, 32 d'
to
10 _
o
as
20
IS
10
.3
5
0 5
, ~13~
4 .5 6
(e)
ll
1~. 11.`
I .
.7 8
9 10
~ HOST SIZES AVAILABLE n- 301
1 1 12 13
~ ~ or\
11~81~
~-
.9 1.0 1.1 1 2 1.3
.4 5 .6 7 .8
SCALE SIZE (mm 2)
FIGURE 3 a-d, size distribution of third-stage California red scale on which Aphytis
melinus laid indicated numbers and sexes of eggs. e-f, size distribution of scale chosen
by and offered to A. melinus for parasitization.
OCR for page 175
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
QPbY~ ingnonensis
5 ~ HOST SIZES YIELDING 20` ~nit 36d.
2 EGGS / HOST (a )
0 ~ .
. 5 .4 .S 6 7 .8 .91.0 1.1 1.2 1 .3
~ HOST SIZES YIELDING As ANDY nets Aid, 13d,
2 EGGS / HOST I
(b)
0 i ~ - ~·a ~ ~ ~ ~
: 5 4 5 6 7 8 9 10 1 1 1.2 1.3
10
S
o
10
5
o
As 20
111
o
15
10
-
O ~
3 .4 .5
HOSTS YIELDING A
I E GO / HOST
n.36 36$
- 11l~l l 1 (C)
. .4 5 .6 7 .8 .9 10 1.1 1.2 1.3
HOSTS YIELDING A J'
I EGG / HOST ,
nil 53 53]
|1' 1 (d)
. 5 4 .5 6 .7 .8 9 1.0 1 1 1.2 1.3
HOST SIZES PARASITIZED nil 164
4gst,72d'
lit,. n
(e)
.S .9 1 0 1.1 1.2 1.3
30
2S
20
15
10
5
~ HOST SIZES AVAILABLE nit 383
3 .. .e .6 7 ~ 9 1 0
SCALE SlZE(mm2)
(I)
111~. .
~ 1 1.2
175
1 ~
FIGURE 4 a-d, size distribution of third-stage California red scale on which Aphytis
lingnanensis laid indicated numbers and sexes of eggs. e-f, size distribution of scale
chosen by and offered to A. Iingnanensis for parasitization.
OCR for page 179
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
179
prey densities are limited by natural enemies, because these agents compete
intraspecifically and interspecifically for hosts or prey. Thus, the agents
are themselves limited by the densities of their prey or hosts in a reciprocal
interaction. However, DeBach and colleagues (DeBach, 1966; DeBach
and Sundby, 1963; Rosen and DeBach, 1979) concluded, on the basis of
laboratory and field experiments, that the two principal parasitoids re-
sponsible for biological control of California red scale were not limited
by host density. But if hosts were not limiting for the parasitoids, how
did Aphytis melinus control California red scale biologically? We used the
principles of foraging theory to identify what scale types the parasitoids
chose as hosts, to rank the scale for quality as hosts in the laboratory,
and to test this ranking in the field. Because Aphytis allocates sons to
small hosts and daughters to large hosts, sex-allocation theory became an
extension of foraging theory. Thus, the hypothesis we tested was an
amalgam of these principles that resources are indeed limiting and that
the limitation is evinced as a male-biased sex ratio in the field population
of A. melinus. As scale grow, they reach the size used by Aphytis to
produce sons before they can attain the size used for daughters. Thus, a
male-biased sex ratio results from a scarcity of hosts large enough to
produce daughters. This pattern might be episodic, depending on the
dynamics of the scale's age structure.
A second body of theory used in the design of the experiments concerns
the effect of temperature on the developmental rate of insects (Wagner et
al., 1984~. An insect's rate of development increases with increasing
temperature (to a maximum), but the relative duration spent in a devel-
opmental stage at a given temperature and the developmental rate of that
stage often differ with developmental stage. These effects, coupled with
the influence of temperature on reproduction, lead to variations in an
insect's age structure as a consequence of temperature variations in the
field. We hypothesized that climatically induced variation in the scale's
age structure, coupled with the requirement of A. melinus and A. Iing-
nanensis for a specific size or large scale on which to produce daughters,
leads to bottlenecks in the availability of suitable hosts and that displace-
ment of A. Iingnanensis by A. melinus occurred during such bottlenecks.
Specific Models
First, we used a simulation model of the life history of California red
scale and its parasitoids that organized information about these organisms
(Luck et al., 1980) and included a modified host-parasitoid model similar
to that of Hassell (19781. This model, which embodied the verbal model
OCR for page 180
180
SELECTED CASE STUDIES
specific to biological control, was inadequate, because biological knowl-
edge was insufficient. Thus, we used the verbal model to predict the field
host-parasitoid interaction. This model specifies that natural enemies re-
duce their host or prey populations to densities at which intraspecific
competition and interspecific competition among the predators and par-
asitoids for prey or hosts reciprocally limit the natural enemies' densities
(DeBach, 1974; Huffaker and Laing, 19721. Because it became clear in
the course of the research that, from the parasitoid's perspective, the scale
was not a homogeneous resource, we used foraging and sex-allocation
theory to define, in the laboratory, both host resource requirements for
A. melinus and A. Iingnanensis progeny production (especially daughters)
and the value of a host to a parental female in terms of the quality of the
daughters (size = fecundity) that the scale produced. Finally, we used a
day-degree model developmental rate of the scale and parasitoid as a
function of temperature (Wagner et al., 1984) to evaluate the effects of
diurnal and seasonal temperature patterns on age structure of California
red scale.
Analog Studies
No other evaluations of the effectiveness of a natural enemy appear to
have used a similar conceptual approach. Most of the available studies
(CIBC, 197 1; Clausen, 1978; Greathead, 1976; Greathead et al., 197 1;
McGuggan and Coppell, 1962; McLeod, 1962; Rao et al ., 1971; Turnbull
and Chant, 1961; Wilson, 1960) at best simply documented success or
failure. Important exceptions were the studies of Wellington (1960, 1964,
1965) and Whitham (1978, 1979, 19801.
Project as Experiment
The California red scale research project was designed to improve the
biological control of California red scale and to test conventional wisdom
as to the attributes that characterize an effective biological control agent,
in this case a parasitoid. Huffaker et al. (1977), Hassell (1978), and Waage
and Hassell (1982) proposed the following attributes as characterizing an
effective biological control agent: high search rates, ability to aggregate
in patches of high host density, close synchrony with the host population,
high degree of host specificity, and sufficient reproductive rate to overtake
and suppress the host population. Because we knew that A. melinus and
A. Iingnanensis were successful biological control agents in part of their
ranges, we began testing them to see whether they had these attributes
and whether A. melinus was better endowed with them.
OCR for page 181
BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
181
We quickly faced the problem of how to measure a high rate of search
or determine whether a parasitoid has a sufficiently high reproductive rate
to overtake its host in the field. Moreover, on the basis of a reproductive-
rate criterion, A. Iingnanensis would be judged the better of the two
parasitoids, because it is the more fecund (DeBach and Sundby, 19631.
Unfortunately, A. Iingnanensis was unable to realize its reproductive ad-
vantage in the form of daughters, because it was more restrictive in its
host (red scale) requirements for daughters than was A. melinus: it required
larger scale. Similar problems arose with several other attributes. Thus,
after our initial effort to measure some of the attributes for A. Iingnanensis
and A. melinus in the laboratory (Kfir and Luck, 1979, 1984; Luck et al.,
1980; Podoler, 1981), we changed our approach and asked what the
specific host requirements were for these two parasitoids with respect to
host stage (instar) and size and the pattern of host availability in the field.
We used the parasitoids' behavior and the size of the daughters to find
the value of a host to the female wasp. On the basis of the results of these
laboratory experiments, we are continuing to test the pattern of resource
use in the field. We are nearing the end of this phase of our research in
late 1985. Thus, we have used a flexible research strategy of hypothesis
formation and testing that incorporates laboratory and field experiments
mixed with computer simulation models of aspects of California red scale
and parasitoid biology.
Expert Judgment
Clearly, a research project of this sort is not undertaken by a single
researcher. First, several colleagues have participated in the evolution and
conduct of the research. Rami Kfir, Haggai Podoler, Devin Carrot, Dani
Blumberg, Dicky Sicki-Yu, Daniel Moreno, W. W. Murdoch, Charles
Kennett, and John Reeves all associated with academic or research in-
stitutions have been involved in various aspects of hypothesis formation,
experimental design, experimental conduct, analysis, and interpretation.
Several persons Harry Griffith, Jim Stewart, Jim Gorden, and Stanley
Warner-with many years of experience in citrus pest management con-
tributed as participants in the research and as critics of our interpretations
of the results. Finally, in response to seminars, in conversations with
colleagues especially F. Galls, J. M. M. van Alphen, J. C. van Lentern,
P. DeBach, L. E. M. Vet, L. Nunny, and D. R. Strong or in peer
reviews of submitted papers, questions or comments often called attention
to an aspect of the problem of which we were unaware or stimulated us
to see the problem from a different perspective. Thus, the project repre-
sents a collage of contributions from a variety of sources.
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SELECTED CASE STUDIES
CONTRIBUTION OF ECOLOGICAL KNOWLEDGE
TO PROJECT RESULTS
Classical biological control has been very much a trial-and-error en-
terprise. It has been based on the notion that natural enemies regulate
phytophagous insect populations and that an effective natural enemy is
well adapted to and synchronized with its host or prey, is a good searcher,
has a high reproductive rate, and aggregates at denser host or prey patches.
The large number of successful biological control projects shows that
natural enemies indeed limit the densities of their host or prey populations.
Yet, if a measure of a successful theory is its ability to predict the outcome
of a particular experiment, then predator-prey theory and biological control
theory are inadequate. We cannot predict whether a given introduction
will succeed or fail. More important, we cannot describe a natural enemy's
attributes that characterize a successful biological control agent. Thus,
predator-prey theory is to a great extent untested and, in its current for-
mulation, not easily falsified. Therefore, we studied a biological control
project in which both successful and unsuccessful parasitoids have been
introduced, so that we could test several hypotheses arising from predator-
prey theory and biological control theory and compare successful and
unsuccessful parasitoids. Theory played a role both in formulating the
hypotheses and in specifying the type of project to look at.
The California red scale biological control project was chosen for several
reasons: the natural histories of the organisms involved were well known,
the history of the project was well documented, the scale is controlled
biologically in only a part of its California range, the scale and its natural
enemies are easily reared in the laboratory, and the parasitoids responsible
for the biological control of the scale are known. Initially, our experimental
designs were guided by the Nicholson-Bailey (1935) model as modified
by Hassell and Varley (Hassell, 19781. Although we obtained a modeled
host-parasitoid interaction that persisted, it provided little insight into why
A. melinus was so successful. The characteristics that defined the host-
parasite interaction could not be measured in the field. Optimal-foraging
theory became an alternative when evidence emerged that A. melinus and
A. Iingnanensis did not use the same host stages for offspring, as DeBach
and co-workers had asserted (DeBach, 19~6; DeBach and Sundby, 1963;
Rosen and DeBach, 19794. Optimal-foraging theory provides ways of
ranking hosts based on their value to the parasitoid, and we were able to
use the size of the female progeny arising from a host as a surrogate
measure of host quality. Thus, foraging theory played a role in refor-
mulating the questions. More important, it led us to stop thinking of the
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BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
183
host-parasitoid interaction as one in which hosts and parasitoids are ho-
mogeneous units (i.e., the old predator-prey theory) and to start thinking
of hosts as resources of different value.
ACKNOWLEDGMENTS
The work described in this study was supported by grants from the
National Science Foundation (BSR 84-03394) and the Binational Agr~-
cultural Research and Development Fund (1-138-791.
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Committee Comment
The first point that emerges from the California red scale case is not
treated in detail by Luck that, even before the study that he describes
was initiated, important partial control of red scale was achieved at little
cost and with little attention to ecological theory (Clausen, 1978; DeBach,
19741. The key new knowledge deployed was taxonomic until 1947,
virtually all Aphytis reared overseas from California red scale were thought
to be A. chrysomphali. Because this species had already been introduced
and had usually not exerted very good control (partly because of pesticides
and ants), specimens attributed to A. chrysomphali were not sent to the
United States. Thus, in 1905-1909, a species that was probably A. Iing-
nanensis was discovered in southern China, but not shipped. With the
recognition of distinct species, A. Iingnanensis was introduced in 1947
and very quickly exerted important control. The ecological knowledge
used later to increase this control was rudimentary autecology. It appeared
that A. Iingnanensis was hindered by the harsh climate of interior southern
California, so a search was initiated for other parasitoids in areas with
similar climate. Success was achieved in northwestern India and Pakistan
with the discovery of A. melinus. This approach is typical of biological
control efforts; the first consideration in the search for natural enemies is
usually that the climate of their native region approximate the climate
where control is sought.
Luck's description is of the effort to extend control to the desert and
the San Joaquin Valley, and his thrust is an interesting mixture of classical
biological control (much like the introduction of the Aphytis species that
are already present) and academic evolutionary ecology. One could simply
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BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
187
have proceeded by trying more and more introductions from many parts
of the world, perhaps focusing the search by looking for areas with citrus
and with climates very similar to those of the desert and the San Joaquin
Valley and hoping that some species would prove effective where the 52
already tried had not. Instead, Luck tried to understand why control op-
erates differently in different regions and why A. melinus is replacing A.
Iingnanensis, despite the greater fecundity of the latter. The goal of this
understanding is either to predict better what sort of parasitoid would
succeed where A. melinus and A. Iingnanensis have failed or to modify
cultivation or other conditions so as to increase the effects of the Aphytis
that are already present.
A number of apparently relevant ecological theories were examined and
incorporated into this effort. For the most part, these proved inspirational
or didactic, rather than directly applicable. The key to the entire biological
control rationale is that the host (red scale) will ultimately be controlled
by the parasitoids and will thus come to be scarce, so that parasitoid
populations will ultimately be limited by intraspecific or interspecific
competition; this is an entomological version of the "green earth" hy-
pothesis of Hairston, Smith, and Slobodkin (19601. Luck observes that
the degree of resolution afforded by this hypothesis did not allow answers
to the most pertinent questions. He thus proceeded to the more specific
traditional predation models of Nicholson and Bailey (1935) and Hassell
and Varley (Hassell, 1978), but found that the model parameters were
ambiguous and unmeasurable and so could not help to explain the geo-
graphic variation in parasitism rate or the apparent replacement of one
parasitoid by another. The key to a more useful approach seems to have
been the recognition that red scale individuals are not a uniform resource
for the wasps, which led rather naturally to casting the problem in terms
of optimal foraging. Although no particular existing optimal-foraging model
was applicable, simply the formulation of the problem in these terms led
to major insights on both geographic variation in parasitism and the su-
periority of A. melinus over A. Iingnanensis. It is also noteworthy that
Luck's familiarity with sex-allocation theory led him to examine sex ratio
as an indicator of degree of competition for large hosts.
In sum, idiosyncrasies of key species in this study rendered even the
most detailed theories inapplicable, but the theories, particularly optimal
foraging, suggested new and fruitful ways of looking at the problem.
Without the massive information on the biology of the organisms, one
could not even have begun the study, but without familiarity with the
theory, the beginnings of a solution might have been much longer in
coming.
The entire project is conceived not only as an attempt to solve a particular
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SELECTED CASE STUDIES
environmental problem, but as an experiment to test hypotheses generated
by various ecological theories and perhaps to aid in modifying the theories
or hypotheses. For example, the intersection of optimal-foraging theory,
competition theory, and sex-allocation theory in the explanation of why
A. melinus outcompetes A. Iingnanensis even when the latter would be
successful by itself is more than just interesting entomology it is an
exciting theoretical advance that should spur further theoretical research.
A quantitative generalization of this intersection does not exist, and the
attention of theorists should be drawn to the problem. Whether the the-
oretical advance can ultimately help to solve the practical environmental
problem noninsecticidal control of red scale in the desert and the San
Joaquin Valley remains to be seen. However, the entire study is certainly
an advance over the trial-and-error approach of much classical biological
control, and the focus on precise mechanisms of species interaction seems
to lend itself to more theoretical treatment.
It is interesting that the scoping of this project, as for all biological
control (and, in fact, for most of applied ecology), is somewhat myopic.
The myriad effects of introduced species are well documented in the
ecological literature (e.g., Elton, 1958; Simberloff, 1981), and biological
control rests fundamentally on introducing species, such as the Aphytis
wasps used to control red scale. Although attention is paid to more than
just the effects on red scale, it is restricted to effects that impinge on
agricultural economy. For example, one wishes to avoid introducing a
parasitoid or predator that attacks a beneficial species, such as a pollinator,
and one screens potential imports to ensure that they are not carrying
hyperparasites that would interfere with the parasites already active in
controlling agricultural pests. However, little attention is paid to the pos-
sible effects of an introduced species on native species that are not agri-
culturally important.
Howarth (1983), for example, laments the reduction of native Hawaiian
lepidopterans, partially by species introduced for biological control. He
calls for a more narrowly focused release effort, rather than the hit-and-
miss release of many potentially beneficial species that typifies some
biological control efforts. The direction that the red scale study has taken
certainly qualifies as a desirable narrowing of focus. Howarth also calls
for more studious consideration of potential effects of control agents on
nontarget species, just as one seeks such effects for pesticides. The three
Aphytis species of most interest in red scale control A. chrysomphali,
A. Iingnanensis, and A. melinus all attack other insects; but, as far as
is known, all the other hosts are themselves agricultural pests, such as
yellow scale and dictyospermum scale (Clausen, 19781. Consequently,
unexpected detrimental effects of their introduction are unlikely. However,
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BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE
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the fact that a successful introduction is virtually impossible to eradicate
(Sailer, 1983) and can easily spread from the site of introduction dictates
a particularly broad scoping process.
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Representative terms from entire chapter:
biological control
