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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

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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

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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.

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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.

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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.

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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

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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

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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

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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.

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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.

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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.

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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

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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.

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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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182 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. REFERENCES Abdelrahman, I. 1974. Studies in the ovipositional behavior and control of sex in Aphytis melinus DeBach, a parasite of California red scale, Aonidiella aurantii (Mask.). Aust. J. Zool. 22:231-247. Bedford, E. C. G., and M. B. Georgala. 1978. Citrus pests in the Republic of South Africa. Sci. Bull. Dept. Agric. Tech. Ser., Rep. S. Afr. 391:109-118. Bodenheimer, F. S. 1951. Citrus Entomology in the Middle East. W. Junk, The Hague. Brown, W. L., Jr., T. Eisner, and R. H. Whittaker. 1970. Allomones and kairomones: Transspecific chemical messengers. BioScience 20:21-22. Charnov, E. L. 1982. The Theory of Sex Allocation. Princeton University Press, Princeton, N.J. Charnov, E. L., R. L. Los-den Hartogh, W. T. Jones, and J. van den Assem. 1981. Sex ratio evolution in a variable environment. Nature 289:27-33. Chewyreuv, I. 1913. Le role des femelles dans la determination du sexe et leur descendance dans le groupe des Ichneumonides. C. R. Soc. Biol. Paris 74:695-699. CIBC (Commonwealth Institute of Biological Control). 1971. Biological Control Pro- grammes Against Insects and Weeds in Canada, 1959-1968. Technical Communication 4. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. Clausen, C. P. 1939. The effects of host size upon the sex ratio of hymenopterous parasites and its relation to methods of rearing and colonization. J. N.Y. Entomol. Soc. 47:1-9. Clausen, C. P. 1978. Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review. USDA/ARS Agric. Handbk. 480. Agricultural Research Service, U. S. Department of Agriculture, Washington, D.C. DeBach, P. 1965. Some biological and ecological phenomena associated with colonizing entomophagous insects. Pp. 287-303 in H. G. Baker and G. L. Stebbins, eds. The Genetics of Colonizing Species. Academic Press, New York. DeBach, P. 1966. The competitive displacement and coexistence principles. Annul Rev. Entomol. 11: 184-212. DeBach, P. 1974. Biological Control by Natural Enemies. Cambridge University Press, New York. DeBach, P., and L. C. Argyriou. 1967. The colonization and success in Greece of some imported species (Hym., Aphelinidae) parasitic on citrus scale insects (Hom., Diaspi- didae). Entomophaga 12:325-342. DeBach, P., and P. Sisojevic. 1960. Some effects of temperature and competition on the

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184 SELECTED CASE STUDIES distribution and relative abundance of Aphytis lingnanensis and A. chrysomph~li (Hy- menoptera: Aphelinidae). Ecology 41: 153-160. DeBach, P., and R. A. Sundby. 1963. Competitive displacement between ecological hom- ologues. Hilgardia 34: 105- 166. Dittrich, V. P., P. Streibert, and P. A. Bathe. 1974. An old case reopened: Mite stimulation by insecticide residues. Environ. Entomol. 3:534-539. Ebeling, W. 1959. Subtropical Fruit Pests. University of California Division of Agricultural Science, Berkeley. Flaherty, D. L., J. E. Pehrson, and C. E. Kennett. 1973. Citrus pest management studies in Tulare County. Calif. Agric. Nov., pp. 3-7. Furness, G. O., G. A. Buchanan, R. S. Georgie, and N. L. Richardson. 1983. A history of the biological and integrated control of red scale, Aonidiella aurantii, on citrus in the lower Murry Valley of Australia. Entomop~aga 28:199-212. Georghiou, G. P., and C. E. Taylor. 1977. Pesticide resistance as an evolutionary phe- nomenon. Proc. Int. Congr. Entomol. 15:759-792. Greathead, D. J., ed. 1976. A Review of Biological Control in Western and Southern Europe. Technical Communication 7. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. Greathead, D. J., J. F. G. Lionnet, N. Lodos, and J. A. Whellan. 1971. A Review of Biological Control in the Ethiopian Region. Technical Communication 5. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. Hassell, M. P. 1978. The Dynamics of Arthropod Predator-Prey Systems. Princeton Uni- versity Press, Princeton, N.J. Hassell, M. P. 1980. Foraging strategies, population models and biological control: A case study. J. Anim. Ecol. 49:603-628. Huffaker, C. B., and J. E. Laing. 1972. "Competitive displacement" without a shortage of resources? Res. Pop. Ecol. 14:1-17. Huffaker, C. B., R. F. Luck, and P. S. Messenger. 1977. The ecological basis of biological control. Proc. Int. Congr. Entomol. 15:560-586. Jones, V. P., and M. P. Parrella. 1984. The sublethal effects of selected insecticides on life table parameters of Panonychus citri (Acari: Tetranychidae). Can. Entomol. 76:1178- 1180. Kfir, R., and R. F. Luck. 1979. Effects of constant and variable temperature extremes on sex ratio and progeny production by Aphytis melinus and A. Iingnanensis (Hymenoptera: Aphelinidae). Ecol. Entomol. 4:335-344. Kfir, R., and R. F. Luck. 1984. Effects of temperature and relative humidity on the developmental rate and adult life span of three Aphytis species (Hym., Aphelinidae) parasitizing California red scale. Z. Angew. Entomol. 97:314-320. Luck, R. F. 1984. Integrated pest management in California citrus. Proc. Int. Soc. Citricul. 2:630-635. Luck, R. F., and H. Podoler. 1985. The potential role of host size in the competitive exclusion of Aphytis lingnanensis by A. melinus. Ecology 66:904-913. Luck, R. F., and N. Uygun. In press. Host recognition and selection by Aphytis species: Response to California red, Aonidiella aurantii (Mask.), oleander, Aspidiotus nerii Bouche, and cactus, Diaspis echinocacti (Bouche) scale cover extracts. Entomol. Exp. Appl. Luck, R. F., R. van den Bosch, and R. Garcia. 1977. Chemical insect control A troubled pest management strategy. BioScience 27:606-611. Luck, R. F., J. C. Allen, and D. Baasch. 1980. A systems approach to research and decision making in the citrus ecosystem. Pp. 366-395 in C. B. Huffaker, ed. New Technology of Pest Control. John Wiley & Sons, New York.

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BIOLOGICAL CONTROL OF CALIFORNIA RED SCALE 185 Luck, R. F., H. Podoler, and R. Kfir. 1982. Host selection and egg allocation behaviour by Aphytis melinus and A. Iingnanensis: A comparison of two facultatively gregarious parasitoids. Ecol. Entomol. 7:397-408. Maggi, V. L., and T. F. Leigh. 1983. Fecundity response of the two-spotted spider mite to cotton treated with methyl parathion or phosphoric acid. J. Econ. Entomol. 75:616- 619. McGuggan, B. M., and H. C. Coppell. 1962. Biological control of forest insects, 1910- 1958. Pp. 35-127 in A Review of the Biological Control Attempts Against Insects and Weeds in Canada. Technical Communication 2. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. McLeod, J. H. 1962. Biological control of pests of crops, fruit trees, ornamentals and weeds in Canada up to 1959. Pp. 1-33 in A Review of Biological Control Attempts Against Insects and Weeds in Canada. Technical Communication 2. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. Moreno, D., and C. E. Kennett. 1985. Predictive year-end California red scale (Homoptera: Diaspididae) orange fruit infestation based on male trap catches in the San Joaquin Valley, California. J. Econ. Entomol. 78:1-9. Nicholson, A. J., and V. A. Bailey. 1935. The balance of animal populations. Proc. Zool. Soc. Lond. 3:551-598. Orphanides, G. M. 1984. Competition displacement between Aphytis spp. [Hym.: Aphel- inidae] parasites of the California red scale in Cyprus. Entomophaga 29:275-281. Pianka, E. R. 1981. Competition and niche theory. Pp. 167-196 in R. M. May, ed. Theoretical Ecology: Principles and Applications. Sinauer Associates, Sunderland, Mass. Podoler, H. 1981. Effects of variable temperatures on responses of Aphytis melinus and A. Iingnanensis to host density. Phytoparasitica 9:179-190. Pyke, G. H., H. R. Pulliam, and E. L. Charnov. 1977. Optimal foraging: A selective review of theory and tests. Q. Rev. Biol. 52:137-154. Quayle, H. J. 1938. Insects of Citrus and Other Subtropical Fruits. Comstock Publ. Co., Ithaca, N.Y. Quednau, F. W., and H. M. Hubsch. 1964. Factors influencing the host-finding and host acceptance pattern in some Aphytis species (Hymenoptera: Aphelinidae). S. Afr. J. Agric. Sci. 7:543-554. Rao, V. P., M. A. Ghani, T. Sankaran, and K. C. Mathur. 1971. A Review of the Biological Control of Insects and Other Pests in South-east Asia and the Pacific Region. Commonw. Inst. Biol. Control Tech. Comm. 6. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. Rosen, D., and P. DeBach. 1978. Diaspididae. Pp. 78-128 in C. P. Clausen, ed. Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review. USDA/ARS Agriculture Handbook 480. Agricultural Research Service, U.S. Department of Agri- culture, Washington, D.C. Rosen, D., and P. DeBach. 1979. Species of Aphytis of the World (Hymenoptera: Aphel- inidae). W. Junk, The Hague. Turnbull, A. L., and D. A. Chant. 1961. The practice and theory of biological control of insects in Canada. Can. J. Zool. 39:697-753. Waage, J. K., and M. P. Hassell. 1982. Parasitoids as biological control agents A fundamental approach. Parasitology 84:241 -268. Wagner, T. L., H. Wu, P. J. H. Sharpe, and R. N. Coulson. 1984. Modeling distributions of insect development time: A literature review and application of the Weibull function. Ann. Entomol. Soc. Am. 77:475-483.

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186 SELECTED CASE STUDIES Wellington, W. G. 1960. Qualitative changes in natural populations during changes in abundance. Can. J. Zool. 38:289-314. Wellington, W. G. 1964. Qualitative changes in populations in unstable environments. Can. Entomol. 96:436-451. Wellington, W. G. 1965. Some maternal influences on progeny quality in the western tent caterpillar, Malacosoma pluviale (Dye). Can. Entomol. 97:1-14. Whitham, T. G. 1978. Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59:1164-1176. Whitham, T. G. 1979. Temtor~al behaviour of Pemphigus gall aphids. Nature 279:324- 325. Whitham, T. G. 1980. The theory of habitat selection: Examined and extended using Pemphigus aphids. Am. Nat. 115:449-466. Wilson, F. 1960. A Review of the Biological Control of Insects and Weeds in Australia and Australian New Guinea. Commonw. Inst. Biol. Control Tech. Comm. 1. Com- monwealth Agricultural Bureaux, Farnham Royal, Slough, Eng. 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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188 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 189 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. References Clausen, C. P. 1978. Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review. USDA/ARS Agriculture Handbook 480. Agricultural Research Ser- vice, U.S. Department of Agriculture, Washington, D.C. DeBach, P. 1974. Biological Control by Natural Enemies. Cambridge University Press, New York. Elton, C. S. 1958. The Ecology of Invasions by Animals and Plants. Methuen, London. Hairston, N. G., F. E. Smith, and L. B. Slobodkin. 1960. Community structure, population control, and competition. Am. Nat. 94:421-425. Hassell, M. P. 1978. The Dynamics of Arthropod Predator-Prey Systems. Princeton Uni- versity Press, Princeton, N.J. Howarth, F. G. 1983. Classical biocontrol: Panacea or Pandora's box? Proc. Hawaii. Entomol. Soc. 24:239-244. Nicholson, A. J., and V. A. Bailey. 1935. The balance of animal populations. Proc. Zool. Soc. Lond. 3:551-598. Sailer, R. I. 1983. History of insect introductions. Pp. 15-38 in C. Graham and C. Wilson, eds. Exotic Plant Pests and North American Agriculture. Academic Press, New York. Simberloff, D. 1981. Community effects of introduced species. Pp. 53-81 in M. H. Nitecki, ed. Biotic Crises in Ecological and Evolutionary Time. Academic Press, New York.