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Selecting effective parasitoids for biological control introductions: Codling moth as a case study
Biological Control 34 (2005) 274–282 www.elsevier.com/locate/ybcon
Selecting eVective parasitoids for biological control introductions: Codling moth as a case study Nick Mills ¤ Insect Biology, Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3112, USA Received 22 December 2004; accepted 23 February 2005 Available online 25 March 2005
Abstract Codling moth is a notorious fruit-boring pest that has been neglected as a target for biological control introductions. Nonetheless, it is a suitable target as it is an exotic species in the western U.S., on an exotic crop plant, in a relatively undisturbed environment, and has a lower level of abundance in its region of origin in Central Asia. In contrast, it belongs to the Olethreutidae, a family of pests with a very poor history of past successes in the biological control record. From an analysis of a stage-structured model for codling moth, the second instar and cocoon are identiWed as the most vulnerable life stages in terms of the potential for additional parasitism-based mortality to reduce the intrinsic rate of increase of codling moth populations. Criteria used in the selection of eVective parasitoids for introduction to the western U.S. from Central Asia were the absence of antagonistic interactions between parasitoid species, greater than 30% parasitism observed in the region or origin, and parasitoids targeting the second instar and cocoon stages. Three species selected for introduction were the larval parasitoid Bassus ruWpes, and two cocoon parasitoids Liotryphon caudatus and Mastrus ridibundus. Of these, M. ridibundus also exhibits three attributes considered to be of value from a theoretical perspective, a positive response to patches of higher host density, a shorter generation time, and production of a greater number of female oVspring per host attacked. 2005 Elsevier Inc. All rights reserved. Keywords: Bassus ruWpes; Cydia pomonella; Liotryphon caudatus; Mastrus ridibundus; Introductions; Parasitism; Parasitoid interactions; Stage-structured model; Western U.S.
1. Introduction The successful biological control of the cottony cushion scale, Icerya purchasi Maskell, as a pest of citrus in southern California in 1889, heralded an explosive interest in the potential of classical biological control as an approach to the long-term management of invasive arthropod pests (Caltagirone and Doutt, 1989). Since this Wrst historical success, more than 100 years ago, California has been one of the most active regions of the world with regard to the pursuit of biological control
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solutions for invasive pests. There have also been numerous subsequent successes in California, including the suppression of invasive armored scales, whiteXies and mealybugs on citrus, as well as other notable cases such as olive scale and walnut aphid (Mills and Daane, 2005). Such successes have also been frequent in many other regions of the world (Greathead, 1995) with such dramatic results as those achieved for suppression of cassava mealybug, Phenacoccus manihoti Matile-Ferrero, across the central belt of Africa through the introduction of the parasitoid, Apoanagyrus lopezi De Santis (Neuenschwander, 2001). While the practice of classical biological control has been questioned in recent years, due to the environmental risks posed by potential direct and indirect non-target
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impacts from the introduced natural enemies (Follett and Duan, 1999; Louda and Stiling, 2004; SimberloV and Stiling, 1996), Hoddle (2004) persuasively argues for the continued role of classical biological control in the Wght against the devastations caused by invasive pests. In this regard, the greatest challenges for biological control practitioners are to be able to identify and select the most eVective candidate control agents from the region of origin of invasive pests, and to minimize the likelihood of undesirable environmental impacts through eVective pre-release studies on the selected biological control agents. Thus in contrast to earlier biological control projects, emphasis in the future will be on minimizing the number of exotic species required to achieve successful biological control (McEvoy and Coombs, 1999), and maximizing the chances of successful suppression of the target pest. By the late 1980s it was evident that through the historical record of classical biological control there had been two extremes among the approaches used to select natural enemies as candidates for biological control introductions. At one extreme, an empirical approach (Ehler, 1990) sought to reconstruct the full natural enemy complex through the introduction of all suitable natural enemies form the region of origin. A good example of this approach has been the biological control program targeting the gypsy moth, Lymantria dispar L., in the northeastern United States, with more than 60 diVerent parasitoid and predator species released into the target environment (Dahlsten and Mills, 1999). The opposite extreme, often referred to as the holistic approach (Waage, 1990), attempted to identify the single best natural enemy species for introduction from the life history and behavioral characteristics of the natural enemies in relation to the demographic nature of the pest. This more theoretical approach to the selection of individual control agents is well exempliWed by the biological control program for the mango mealybug, Rastrococcus invadens Williams (Godfray and Waage, 1991). Here I will discuss codling moth, Cydia pomonella (L.), as a target for classical biological control, and the rationale that we have taken in selecting parasitoids for introduction into the western United States (California and Washington) for the classical biological control of this long-established invasive pest. Codling moth provides a valuable case study to illustrate some of the diYculties that a biological control practitioner faces in addressing the potential for success and the selection of candidate control agents.
2. Codling moth as a target for classical biological control Codling moth is a notorious fruit-boring pest that has extended its original distribution from the natural apple forests of Central Asia to cover all apple growing
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regions of the world, with the exception of eastern China and Japan. Recent interest in germplasm stocks from around the world, combined with the development of molecular markers, has demonstrated the ancestral role of Central Asia as the region of origin of the domestic apple (Geibel et al., 2000; Harris et al., 2002). While no comparable study has been made of the genetic structure of codling moth populations from around the world, it seems likely that the very close association of codling moth with apples would also point to Central Asia as a region of origin of this pest. In addition, although codling moth has frequently been recorded as a pest of pears, Asian pears, walnuts, and occasionally apricots, peaches, and plums (Barnes, 1991), it has only been recorded from these host plants in cultivated orchards. This suggests that it is the modern cultivars rather than the wild progenitors of these other tree crops that have been incorporated into the host plant range of codling moth as it expanded its distribution around the world. Codling moth Wrst appeared in the western United States in California in 1872 (Simpson, 1903), and has since become a devastating pest of apples causing almost complete crop loss in the absence of eVective management, and up to 40% loss of early-harvest pear cultivars and early-harvest walnut cultivars (Barnes, 1991; Mills, unpublished observations). As a potential target for classical biological control, the codling moth might be considered to rank very low in terms of the chances for success. One reason for this is that from the historical record of classical biological control introductions, as documented by the BIOCAT database (Greathead and Greathead, 1992), the rate of success for olethreutid moths has been particularly low in comparison with other families of pests (Fig. 1). In addition, as a fruit borer, codling moth is a direct pest that directly damages the harvestable part of the crop and thus even low densities of codling moth frequently
Fig. 1. The rate of success in classical biological control, estimated as the proportion of introduced parasitoid species that have resulted in partial to complete control of the target pest (using the single most optimistic outcome in cases of multiple records of introductions in diVerent regions), in relation to family of the pest (after Mills, 2000).
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exceed the economic injury level. From early on, Lloyd (1960a) recognized that direct pests have a far lower potential for success in classical biological control in comparison to indirect pests which can be tolerated more readily at low densities in the crop. Similarly, as a demand-side pest, feeding on fruiting structures that act as sinks rather than sources of photosynthate, the dynamics of codling moth populations might be expected to be little inXuenced by the action of natural enemies (Gutierrez, 1996). In contrast, one of the most valuable indicators of the potential for success in biological control is a much lower level of abundance of the target pest in its region of origin (Mills, 1990). Although codling moth is well known in Central Asia (Zlatanova, 1987), it is sporadic and far less abundant in natural apple forests, and also less abundant in orchards. This is in part due to the occurrence of only two generations per year in Central Asia in contrast to three generations per year in regions that have a longer growing season, such as California. Nonetheless, over a 4-year period of foreign exploration visits toward the end of the Wrst generation of codling moth in late June from 1996 to 1999, fruit damage in untreated experimental orchards in the region around Almaty in Kazakstan varied from 0 to 5% in comparison to 25–62% damage for the same generation in untreated organic orchards in California over the same time period (Mills, unpublished observations). While this diVerence in relative pest abundance between regions may have been due to a variety of factors unrelated to parasitism, in contrast to a situation of no diVerence in pest abundance between regions, it does not rule out a possible role for biological control. In addition, from an analysis of the biological control record, rates of success in the biological control of invasive insect pests have been greatest for exotic versus native plants, trees versus herbaceous plants, and cultivated versus natural ecosystems (Hawkins et al., 1999). Thus orchard crops, such as pome fruit and walnut orchards in the western United States, have good potential for success as they are characterized by exotic plants, supporting a reduced assemblage of insect herbivores in relation to native plants, cultivated ecosystems, with limited food web connectance and complexity in relation to natural ecosystems, and a tree crop environment, generating less disturbance than an annual row crop (Fig. 2). Finally, in any assessment of the suitability of an invasive pest as a target for classical biological control it is important to consider the economic value of the crops aVected by the pest and the potential for environmental beneWts from reduced use of insecticides. For the western region in 2002 apple production covered almost 200,000 acres generating an annual revenue of $1147 million, pears were grown on 69,000 acres with an annual revenue of $248 million, and walnuts were grown on 200,000 acres with an annual revenue of $305 million (Anon.,
Fig. 2. The rate of success in classical biological control (as deWned in Fig. 1) in relation to region of origin and architectural complexity of the crop plant, and degree of management of the ecosystem (after Hawkins et al., 1999).
2003). In addition, in 2001, damage suppression in apples and pears required from 1.8 to 6.4 and 1.5 to 2.0 applications of azinphos-methyl, respectively, whereas walnuts required 1.3 applications of chlorpyrifos (Anon., 2002). Thus codling moth is a key pest of fruit and nut production in the western U.S. both in terms of potential crop loss and insecticide usage.
3. Stage-structured model of codling moth population growth Codling moth, in common with other lepidopteran hosts, supports a rich assemblage of parasitoid species clustered into parasitoid guilds (sensu Mills, 1994a) that attack the host at successive stages in the life cycle and diVer in mode of development. What is the likelihood that a parasitoid that attacks a particular stage in the life cycle could provide suYcient suppression of codling moth populations to be successful as a biological control agent? Surprisingly, there have been few attempts to analyze the role of parasitism at diVerent stages in the life cycle of a pest in the suppression of pest population growth (but see Lin and Ives, 2003; Murdoch et al., 2003). Using a simple stage-structured model of parasitism of an aphid population, Lin and Ives (2003) found that as a result of removal of those individuals with the greatest reproductive value in the host population, parasitism of larger aphids caused a greater reduction in host population growth rate than parasitism of smaller aphids. Using a similar approach, we can assess the relative importance of parasitism at diVerent stages in the
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life cycle of codling moth through the development of a stage-structured population growth model. A stage-structured matrix model captures both the transition probabilities of individuals moving through the successive life stages, as determined by their respective development rates, and the survivorship of individuals within each stage. The matrix was parameterized for codling moth using fecundity and survivorship data for adults from Geier (1963) and Hagley (1972), egg development rate data from Geier (1963), larval, and cocoon development rate data from Setyobudi (1989), and egg, larval and cocoon survivorship data from Geier (1963) and Wearing (1975). The resultant projection matrix (Table 1) consists of a set of upper diagonal elements (Pi) representing the probability of an individual surviving and transitioning to the subsequent life stage, and a set of lower diagonal elements (Gi) representing the probability of an individual surviving and remaining in that life stage. These probabilities are dependent upon the survival (i) and the development (i) rates of each life stage (i) in relation to the time step of the projection (in this case 1 day), such that Pi D i (1 ¡ i) and Gi D ii. Finally, the top right element of the projection matrix represents the rate of fecundity (Fi), or more speciWcally, the product of the per capita oviposition rate per time step and the proportion of females in the adult stage. Following Caswell (2001), in the absence of parasitism, the projection matrix generates an intrinsic rate of increase for the codling moth population of r D 0.0272 and a population doubling time of 25.44 days. To assess the likelihood that parasitism occurring at a particular stage in the life cycle could be successful in the suppression of codling moth population growth, two diVerent approaches were taken; an analysis of the sensitivity of population growth to the stage-speciWc survivorship elements, and an analysis of the stage-speciWc rate of parasitism needed to reduce the intrinsic rate of increase to zero. The sensitivity of the codling moth model to its component vital rates is best analyzed through their corresponding elasticities, representing the proportional change in population growth that results from a
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proportional change in a particular vital rate. Elasticities depend not only on the reproductive value (vi) of individuals at that stage in the life cycle, but also on their rates of development (i) and survivorship (i). In a stage-structured model the elements of the projection matrix are the transition probabilities (Pi and Gi) for each stage, and the associated elasticities can readily be decomposed to estimate the contributions to population growth of both survivorship (i) and development (i) at each life stage (Caswell, 2001). The resultant elasticities for stage-speciWc survivorship indicate that, for the life stages that are susceptible to parasitism, the greatest responses occur in the Wfth instar and cocoon stages with some responsiveness also at the egg and second instar stages (Table 2). A corresponding analysis of the daily stage-speciWc rates of parasitism needed to reduce the intrinsic rate of increase of the codling moth population to zero shows a very similar pattern with 21.0 and 28.4% for Wfth instar and cocoon stages, and 34.6 and 36.3% for egg and second instar stages (Table 2). This analysis of the vulnerability of the codling moth life cycle to added parasitism provides two valuable insights. First, it suggests that codling moth population growth is most vulnerable to additional mortality at the Wfth instar or cocoon stage in its life cycle, and thus that parasitoids attacking these stages might be more Table 2 Analysis of the stage-structured population model for codling moth indicating the relative reproductive value (vi), the elasticities for survivorship (ei), and the daily percent parasitism required to achieve zero population growth (r D 0)
Egg L1 L2 L3 L4 L5 Cocoon Adpr Adr
vi
ei
Percent parasitism
0.016 0.024 0.049 0.060 0.067 0.072 0.150 0.269 0.293
0.073 0.034 0.067 0.036 0.021 0.101 0.151 0.032 0.185
34.6 47.8 36.3 48.4 59.2 28.4 21.0
Table 1 The projection matrix of the stage-structured population model for codling moth
Egg L1 L2 L3 L4 L5 Cocoon Adpr Adr
Egg
L1
L2
L3
L4
L5
Cocoon
Adpr
Adr
0.826 0.138 0.000 0.000 0.000 0.000 0.000 0.000 0.000
0.000 0.700 0.157 0.000 0.000 0.000 0.000 0.000 0.000
0.000 0.000 0.813 0.178 0.000 0.000 0.000 0.000 0.000
0.000 0.000 0.000 0.692 0.299 0.000 0.000 0.000 0.000
0.000 0.000 0.000 0.000 0.523 0.467 0.000 0.000 0.000
0.000 0.000 0.000 0.000 0.000 0.870 0.076 0.000 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.913 0.064 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.665 0.332
1.767 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.931
The elements in the upper diagonal are the probabilities of an individual transitioning from stage i to stage i + 1 (Pi), and the elements in the lower diagonal are the probabilities of an individual remaining in stage i (Gi) in the time step from t to t + 1. Life cycle stages include Li as larval instars, and Adpr and Adr as pre-reproductive and reproductive adults.
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eVective in the biological control of this pest than parasitoids attacking other life stages. Second, it also suggests that the egg and second instar stages could also be vulnerable to additional parasitism.
4. Comparison of parasitoid assemblages in North America and Eurasia Parasitoids of codling moth are readily collected by trapping larvae as they exit attacked fruit and descend the limbs to seek cocooning sites under the bark of the trunk. Parasitoid species reared from Weld collections of codling moth larvae and pupae trapped in 7.5 cm wide corrugated cardboard bands wrapped around the trunks and limbs of apple, pear, and walnut trees in a variety of organic or unsprayed orchards throughout California during the period 1992–2002 are shown in Fig. 3A. Also included in Fig. 3A is Trichogramma platneri Nagarkatti (Trichogrammatidae), an egg parasitoid that has been consistently reared from both naturally laid and experimentally expose codling moth eggs (Mills, 2003a). No attempt was made to collect parasitoids from larvae within fruit, and thus it is possible that we may have overlooked larval ectoparasitoids such as Eulophidae and Bethylidae. In contrast to an earlier survey of codling moth parasitoids in California (Lloyd, 1944), tachinid parasitoids were absent from our rearings, but Coccygomimus hesperus Townes (Ichneumonidae) was recorded as a true pupal
parasitoid. It is also notable that Ascogaster quadridentata Wesm. (Braconidae) was found only in apples, Macrocentrus ancylivorus Rowher (Braconidae) only in walnuts in the Central Valley, and Mastrus carpocapsae (Cushman) (Ichneumonidae) and C. hesperus were conWned to apple in coastal orchards. The only hyperparasitoid in the assemblage was Dibrachys cavus (Walker) (Pteromalidae), a Holarctic species that develops within the cocoons of primary parasitoids within the codling moth cocoon. The majority of these parasitoids are indigenous to California with the exception of A. quadridentata, a Palearctic species that was purposefully introduced into Washington state in the 1920s (Lloyd, 1960b). Codling moth has two generations per year in coastal California and three per year in the Central Valley. In general, levels of parasitism of codling moth were low and typically less than 5% in all areas (Mills, unpublished observations). However, egg parasitism by T. platneri frequently rose to 30–60% later in the season in unsprayed orchards, and parasitism of overwintering cocoons by M. carpocapsae was recorded to be as high at 23% in 1995 in one apple orchard on the Central Coast. The corresponding parasitoid assemblage in the Palearctic region (Fig. 3B) was investigated through trap banding of unsprayed apple trees in the regions around Changins in southwestern Switzerland and around Vienna in eastern Austria from 1992 to 1994, in the region around Almaty in southern Kazakstan from 1995 to 1998, and in the Illi Valley (Xinjiang Province) of
Fig. 3. The parasitoid assemblage associated with codling moth in (A) California, and (B) Eurasia. The circle represents the life cycle of the codling moth with YL, young instar larva; LL, late instar larva; and Coc, cocoon. The arrows represent the life stages attacked and killed by the associated parasitoids, those remaining outside of the circle being ectoparasitoids, and those passing through the circle being endoparasitoids.
N. Mills / Biological Control 34 (2005) 274–282
northwestern China from 1999 to 2003. Trapping in these surveys was primarily conWned to the Wrst generation of codling moth cocooning in June, with more limited sampling at the end of the season in each region. Although codling moth eggs were not sampled during these surveys for parasitoids of codling moth in Eurasia, it is well known that Trichogramma species do occur throughout the region (Dyadechko et al., 1975; Hassan, 1989; Zlatanova and Tarabaev, 1985), and thus a generic Trichogramma sp. has been added to Fig. 3B for completeness. Similarly, while no sampling of larvae within fruit was conducted during these surveys, Hyssopus pallidus (Askew) (Eulophidae) has been added to Fig. 3B, due to its known occurrence in France and Switzerland (Tschudi-Rein et al., 2004). Although most of the parasitoid species occurred on codling moth throughout the regions sampled, Bassus conspicuus (Wesm.) (Braconidae) and Trichomma enecator Rossi (Ichneumonidae) were found only in eastern Austria and southwestern Switzerland, A. quadridentata was absent from northwestern China, and Mastrus ridibundus (Grav.) (Ichneumonidae) occurred only in southern Kazakstan and northwestern China. In addition, although Bassus ruWpes (Nees) occurred both in Europe and Central Asia, it was much more consistent in the latter region. It should also be noted that the Liotryphon species found in Europe is L. caudatus (L.), while that found in Central Asia is a morphologically distinct but unidentiWed Liotryphon species. In addition to D. cavus, a second hyperparasitoid in the Eurasian parasitoid assemblage is Perilampus tristis Mayr (Perilampidae) that develops within the primary parasitoid larvae of A. quadridentata and B. ruWpes. These parasitoid assemblages are very similar to those recorded previously from Europe (e.g., Diaconu et al., 2000; Rosenberg, 1934; Simmonds, 1945), and for Central Asia (Durdyev, 1987; Zlatanova, 1987; Zlatanova and Tarabaev, 1985). One notable diVerence, however, was the presence of Pristomerus vulnerator Panz. (Ichneumonidae) in both southern Kazakstan and northwestern China, although it was absent in previous studies. Codling moth typically produces two generations per year in both the European and Central Asian regions
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that were surveyed in this study. However, the maximum levels of parasitism recorded from the trap bands in individual orchards diVered between the two regions. In Europe the highest rates of parasitism were recorded for A. quadridentata and P. vulnerator (Table 3). In contrast, in southern Kazakstan and northwestern China, both B. ruWpes and M. ridibundus were responsible for the greatest rates of parasitism.
5. Selecting eVective parasitoid species for introduction into the Western United States In response to concerns regarding the environmental risks of biological control, recent biological control projects have focused on host speciWcity as the main criterion for the selection of parasitoids for introduction. In addition to host speciWcity, which is directed toward minimizing the risk of non-target impacts, it is equally important to consider parasitoid eVectiveness and the potential to maximize the chances of successful suppression of the target pest. In view of this, we focus here on parasitoid eVectiveness, and the role of interactions and performance as indicators of success, rather than on host speciWcity, although the latter has also been addressed for this project (Unruh and Mills, unpublished observations). Our initial criteria for the selection of the most eVective parasitoid species for introduction into the western U.S. followed the guidelines suggested by Mills (1990). Of greatest concern was to select parasitoids that showed no evidence of antagonistic interactions. For this reason P. vulnerator was rejected, as it was known from an earlier project on the classical biological control of the European pine shoot moth Rhyacionia buoliana (Denis & SchiV.), that an unidentiWed Pristomerus species functioned as a cleptoparasitoid (Schroeder, 1974). As cleptoparasitism can be diYcult to recognize (Schroeder, 1974), and yet was considered to be one of the key reasons why Orgilus obscurator Nees was unable to successfully control European pine shoot moth in Canada (Dahlsten and Mills, 1999), the possibility of cleptoparasitism in the genus Pristomerus was considered suYcient reason to
Table 3 Maximum percent parasitism rates recorded in individual orchards (with sample sizes of greater than 60 host individuals) for the primary parasitoids collected from banding apple trees in Europe (western Switzerland and eastern Austria) and Central Asia (southern Kazakstan and northwestern China, Xinjiang Province) Europe
Ascogaster quadridentata Bassus conspicuus Bassus ruWpes Pristomerus vulnerator Trichomma enecator Liotryphon spp. Mastrus ridibundus
Central Asia
Switzerland 1992–1993
Austria 1992–1994
Kazakstan 1995–1998
Xinjiang 1999–2003
10.3 — 0.7 32.4 9.9 1.5 —
42.6 3.2 — 27.9 7.4 1.4 —
14.5 — 33.3 3.1 — 3.7 43.9
— — 13.6 0.6 — 4.1 1.4
280
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reject P. vulnerator despite the fact that it remains unknown whether this particular species is cleptoparasitic within the codling moth parasitoid assemblage. As a larval ectoparasitoid, H. pallidus exhibits rapid larval development (Zaviezo and Mills, 1999) which conveys a competitive advantage through a priority eVect over larval endoparasitoids that show protracted larval development (see Mills, 2003b, for further details of parasitoid interactions). As there is some evidence from the literature that lepidopteran parasitoid assemblages that include a greater species richness of larval ectoparasitoids show a reduced richness of larval endoparasitoids (Mills, 1994b), H. pallidus was also considered a potential antagonist. From a more detailed analysis of the interaction of H. pallidus and A. quadridentata it was shown that not only does H. pallidus have competitive superiority, but also that it experiences a distinct Wtness advantage from parasitizing host larvae previously parasitized by A. quadridentata (Zaviezo and Mills, 2001). The Wtness gain by H. pallidus from multiparasitism was considered functionally similar to cleptoparasitism (Mills, 2003b) and suYcient reason to reject this species from consideration as a biological control agent for codling moth. Additional criteria used in the selection of eVective candidates from the Eurasian parasitoid assemblage of codling moth were level of parasitism, and vulnerability of the codling moth life cycle (see Section 3). Hawkins and Cornell (1994) have shown that the likelihood of success in classical biological control is directly related to the extent of parasitism that occurs in the region of origin, with a threshold for success of approximately 30% parasitism. In addition, the earlier analysis of a stage-structured model for codling moth suggested the greater vulnerability of population growth to additional mortality in the second instar and cocoon stages. Using these combined criteria, the larval endoparasitoid B. ruWpes, and the two prepupal ectoparasitoids Liotryphon spp. and M. ridibundus were selected for further consideration. B. ruWpes was recognized as an important parasitoid of codling moth in Kazakstan by Zlatanova (1970) and was the only young larval parasitoid to achieve suYcient levels of parasitism in the surveys conducted in Central Asia (Table 3). Although only one of the two prepupal parasitoids, M. ridibundus, was also dominant in terms of levels of parasitism observed from surveys in Central Asia (Table 3), both were selected as they attack the vulnerable cocoon stage in the life cycle. As cocoon parasitoids, Liotryphon spp. and M. ridibundus could act as facultative hyperparasitoids of primary parasitoid cocoons, such as those of B. ruWpes and A. quadridentata. However, in no-choice tests, neither L. caudatus nor M. ridibundus showed evidence of facultative hyperparasitism (Unruh and Mills, unpublished observations). In view of these results, B. ruWpes, L. caudatus, and M. ridibundus were considered potential candidates for introduction into the western U.S.
A variety of additional traits have been suggested as potential criteria for selection of the ‘best’ parasitoid species for biological control introductions (HuVaker et al., 1977; Kimberling, 2004; May and Hassell, 1988; Murdoch et al., 2003). As summarized by Murdoch et al. (2003), from a theoretical perspective, all else being equal, desirable parasitoid attributes include a higher rate of successful search, a shorter generation time, a preference for patches of higher host density, an absence of host refuges, a preference for host stages of longer duration or that suVer less background mortality, and a greater number of female oVspring produced per attacked host. However, it is clear that trade-oVs have occurred in the evolution of parasitoid life history traits, and that any particular trait may be accompanied by a suite of others that may be less desirable. As a result this reductionist approach has led to few, if any, general principles to guide the selection of the ‘best’ parasitoid species for introduction. Nonetheless, it is worth noting that of the three parasitoids selected above as potential candidates for introduction against codling moth, M. ridibundus exhibits the greatest range of desirable attributes. These include a positive response to patches of higher host density (Bezemer and Mills, 2001), a shorter generation time than its host, allowing it to complete at least two generations on diapausing cocoons of codling moth in the fall (Mills et al., 2004), and gregarious development with the production of an average of 2.4 females per attacked host (Bezemer and Mills, 2003).
6. Conclusions Although considered a target for classical biological control both in the 1920s and again in the early 1960s (Lloyd, 1960b), codling moth has been ignored more recently by biological control practitioners due to the fact that it is a direct pest. As a result codling moth remains a key pest of fruit and nut production in the western U.S. causing substantial crop losses and necessitating continued reliance on within-season insecticide applications to achieve adequate control. A need to reduce insecticide residues in fruit crops (e.g., Melnico, 1999; Smith, 2001) prompted this more detailed analysis of the potential for biological control of codling moth and the selection of parasitoid species for importation from Central Asia. Our analysis focused on orchards as a suitable environment for biological control success, the lower level of abundance of the pest in its region of origin, and the selection of parasitoid species that both avoid the potential for antagonistic interactions and target the vulnerable second instar and cocoon stages of the life cycle. As a result of this approach, the three parasitoids B. ruWpes, L. caudatus, and M. ridibundus were imported
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and released at numerous locations in both California and Washington (Unruh and Mills, unpublished observations). The outcome of these releases is that B. ruWpes has yet to be recovered, L. caudatus has at least temporarily established in California, and M. ridibundus has been recovered from numerous sites in both states and appears to be well established. Codling moth damage in walnuts in California has declined since the release of M. ridibundus in 1996 with parasitism of overwintering cocoons reaching 70% in some unsprayed orchards (Mills, unpublished observations). The outcome of the project cannot be considered a dramatic success, as should be expected in the case of a direct pest (Lloyd, 1960a), but as noted by Goldson et al. (1994), the value of parasitism and the contribution of partial biological control to the overall management of such notorious and intractable pests as the codling moth should not be underestimated. Thus codling moth as a case study in the selection of parasitoid species for introduction in a biological control program for an invasive pest, suggests that there is considerable merit in the use of a more holistic approach. First, a suYcient understanding of the dynamics of the target pest population can be informative in identifying the most vulnerable life stages. Second, a suYcient understanding of the biology of the parasitoids occurring in the region of origin of a target pest is necessary to avoid the potential for antagonistic interactions among selected parasitoid species, particularly when the pest is holometabolous and supports a more complex parasitoid assemblage. A more recent theoretical analysis has further suggested the importance of niche overlap in selecting eVective parasitoids for introduction (Pedersen and Mills, 2004). The occurrence of spatial, temporal or behavioral refuges from parasitism can allow individuals in a pest population to escape from attack by an introduced parasitoid. Consequently, the identiWcation of an additional parasitoid species that can break the host refuge from parasitism provides a powerful opportunity to achieve greater success in biological control. Thus, although biological control has been considered more of an art than a science, the development of a stronger scientiWc basis for the selection of eVective parasitoids for introduction can be used to maximize the potential impact of parasitism for those intractable target pest groups, such as fruit pests, that have historically shown low rates of success in biological control.
Acknowledgments Funding for this project was provided by the Walnut Marketing Board and the Pear Research Advisory Board of California, and the National Research Initiative of the USDA CSREES, Grant No. 0012862.
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Hawkins, B.A., Cornell, H.V., 1994. Maximum parasitism rates and successful biological control. Science 266, 1886. Hawkins, B.A., Mills, N.J., Jervis, M.A., Price, P.W., 1999. Is the biological control of insects a natural phenomenon? Oikos 86, 493–506. Hoddle, M.S., 2004. Restoring balance: using exotic species to control invasive exotic species. Conserv. Biol. 18, 38–49. HuVaker, C.B., Luck, R.F., Messenger, P.S., 1976. The ecological basis of biological control. In: Proc. XV Int. Congr. Entomol., vol. 1976, pp. 560–586. Kimberling, D.N., 2004. Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biol. Invasions 6, 301–318. Lin, L.A., Ives, A.R., 2003. The eVect of parasitoid host-size preference on host population growth rates: an example of Aphidius colemani and Aphis glycines. Ecol. Entomol. 28, 542–550. Lloyd, D.C., 1944. A study of the codling moth and its parasites in California. Sci. Agr. 24, 456–473. Lloyd, D.C., 1960a. SigniWcance of the type of host plant crop in successful biological control of insect pests. Nature 187, 430–431. Lloyd, D.C., 1960b. A Memorandum on Natural Enemies of the Codling Moth, Cydia Pomonella (L.). Commonwealth Institute of Biological Control, Farnham Royal, UK 40pp. Louda, S.M., Stiling, P., 2004. The double-edge sword of biological control in conservation and restoration. Conserv. Biol. 18, 50–53. May, R.M., Hassell, M.P., 1988. Population dynamics and biological control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 318, 129–170. Melnico, R., 1999. Crop proWle for apples in California. Available from:. McEvoy, P.B., Coombs, E.M., 1999. Biological control of plant invaders: regional patterns, Weld experiments and structured population models. Ecol. Appl. 9, 387–401. Mills, N.J., 1990. Biological control, a century of pest management. Bull. Entomol. Res. 80, 359–362. Mills, N.J., 1994a. Biological control: some emerging trends. In: Leather, S.R., Watt, A.D., Mills, N.J., Walters, K.F.A. (Eds.), Individuals, Populations and Patterns in Ecology. Intercept, Andover, UK, pp. 213–222. Mills, N.J., 1994b. Parasitoid guilds: a comparative analysis of the parasitoid communities of tortricids and weevils. In: Hawkins, B.A., Sheehan, W. (Eds.), Parasitoid Community Ecology. Oxford University Press, Oxford, pp. 30–46. Mills, N.J., 2000. Biological control: the need for realistic models and experimental approaches to parasitoid introductions. In: Hochberg, M.E., Ives, A.R. (Eds.), Parasitoid Population Biology. Princeton University Press, Princeton, NJ, pp. 217–234. Mills, N.J., 2003a. Augmentation in orchards: improving the eYcacy of Trichogramma inundation. In: Van Driesche, R. (Ed.), 1st International Symposium on Biological Control of Arthropods. USDA Forest Service FHTET-03-05, pp. 130–135. Mills, N.J., 2003b. Parasitoid interactions and biological control. In: Van Driesche, R. (Ed.), 1st International Symposium on Biological Control of Arthropods. USDA Forest Service FHTET-03-05, pp. 108–113.
Mills, N.J., Daane, K.M., 2005. Nonpesticide alternatives can suppress agricultural pests. Calif. Agric. 59 (1), 23–28. Mills, N.J., Hougardy, E., Julier, E., Pickel, C., Bentley, W., Grant, J., Wulfert, S. 2004. Enhancing the biological control of codling moth in walnuts. Walnut Research Reports 2003, Walnut Marketing Board, Sacramento, CA, pp. 321–331. Murdoch, W.W., Briggs, C.J., Nisbet, R.M., 2003. Consumer-resource Dynamics. Princeton University Press, Princeton, NJ. Neuenschwander, P., 2001. Biological control of the cassava mealybug in Africa: A review. Biol. Control 21, 214–229. Pedersen, B.S., Mills, N.J., 2004. Single vs. multiple introduction in biological control: the roles of parasitoid eYciency, antagonism and niche overlap. J. Appl. Ecol. 41, 973–984. Rosenberg, H.T., 1934. The biology and distribution in France of larval parasites of Cydia pomonella L. Bull. Entomol. Res. 25, 201–256. Schroeder, D., 1974. A study of the interactions between the internal larval parasites of Rhyacionia buoliana (Lepidoptera: Olethreutidae). Entomophaga 19, 145–171. Setyobudi, L., 1989. Seasonality of codling moth, Cydia pomonella L. (Lepidoptera: Olethreutidae) in the Willamette Valley of Oregon: role of photoperiod and temperature. Ph.D. dissertation, Oregon State University, 138pp. SimberloV, D., Stiling, P., 1996. How risky is biological control?. Ecology 77, 1965–1974. Simmonds, F.J., 1945. Observations on the parasites of Cydia pomonella L. in southern France. Sci. Agr. 25, 1–30. Simpson, C.B., 1903. The codling moth. USDA, Division of Entomology, Bulletin No. 41, 1–105. Smith, T.J., 2001. Crop proWles for apples in Washington. Available from:. Tschudi-Rein, K., Brand, N., Kuhrt, U., Dorn, S., 2004. First record of Hyssopus pallidus (Askew, 1964) for Switzerland (Hymenoptera: Eulophidae). Rev. Suisse Zool. 111, 671–672. Waage, J.K., 1990. Ecological theory and the selection of biological control agents. In: Mackauer, M., Ehler, L.E., Roland, J. (Eds.), Critical Issues in Biological Control. Intercept, Andover, UK, pp. 135–157. Wearing, C.H., 1975. Integrated control of apple pests in New Zealand. 2. Field estimation of Wfth-instar larval and pupal mortalities of codling moth by tagging with cobalt-58. N. Z. J. Zool. 2, 135–149. Zaviezo, T., Mills, N.J., 1999. Aspects of the biology of Hyssopus pallidus (Hymenoptera: Eulophidae), a parasitoid of the codling moth (Lepidoptera: Olethreutidae). Environ. Entomol. 28, 748–754. Zaviezo, T., Mills, N.J., 2001. The response of Hyssopus pallidus to hosts previously parasitized by Ascogaster quadridentata: heterospeciWc discrimination and host quality. Ecol. Entomol. 26, 91–99. Zlatanova, A.A., 1970. Biology of Microdus ruWpes Nees (Hymenoptera, Braconidae), a parasitoid of codling moth in Kazakhstan. Entomol. Obozr. 49, 749–755. Zlatanova, A.A., 1987. The codling moth. Zashch. Rast. Moskva 11, 54. Zlatanova, A.A., Tarabaev, Ch.K., 1985. Natural enemies and their signiWcance in the control of the codling moth, Laspeyresia pomonella L. (Lepidoptera, Tortricidae) in south-eastern Kazakhstan. Entomol. Obozr. 64, 510–515.
Selecting eVective parasitoids for biological control introductions: Codling moth as a case study Nick Mills ¤ Insect Biology, Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3112, USA Received 22 December 2004; accepted 23 February 2005 Available online 25 March 2005
Abstract Codling moth is a notorious fruit-boring pest that has been neglected as a target for biological control introductions. Nonetheless, it is a suitable target as it is an exotic species in the western U.S., on an exotic crop plant, in a relatively undisturbed environment, and has a lower level of abundance in its region of origin in Central Asia. In contrast, it belongs to the Olethreutidae, a family of pests with a very poor history of past successes in the biological control record. From an analysis of a stage-structured model for codling moth, the second instar and cocoon are identiWed as the most vulnerable life stages in terms of the potential for additional parasitism-based mortality to reduce the intrinsic rate of increase of codling moth populations. Criteria used in the selection of eVective parasitoids for introduction to the western U.S. from Central Asia were the absence of antagonistic interactions between parasitoid species, greater than 30% parasitism observed in the region or origin, and parasitoids targeting the second instar and cocoon stages. Three species selected for introduction were the larval parasitoid Bassus ruWpes, and two cocoon parasitoids Liotryphon caudatus and Mastrus ridibundus. Of these, M. ridibundus also exhibits three attributes considered to be of value from a theoretical perspective, a positive response to patches of higher host density, a shorter generation time, and production of a greater number of female oVspring per host attacked. 2005 Elsevier Inc. All rights reserved. Keywords: Bassus ruWpes; Cydia pomonella; Liotryphon caudatus; Mastrus ridibundus; Introductions; Parasitism; Parasitoid interactions; Stage-structured model; Western U.S.
1. Introduction The successful biological control of the cottony cushion scale, Icerya purchasi Maskell, as a pest of citrus in southern California in 1889, heralded an explosive interest in the potential of classical biological control as an approach to the long-term management of invasive arthropod pests (Caltagirone and Doutt, 1989). Since this Wrst historical success, more than 100 years ago, California has been one of the most active regions of the world with regard to the pursuit of biological control
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solutions for invasive pests. There have also been numerous subsequent successes in California, including the suppression of invasive armored scales, whiteXies and mealybugs on citrus, as well as other notable cases such as olive scale and walnut aphid (Mills and Daane, 2005). Such successes have also been frequent in many other regions of the world (Greathead, 1995) with such dramatic results as those achieved for suppression of cassava mealybug, Phenacoccus manihoti Matile-Ferrero, across the central belt of Africa through the introduction of the parasitoid, Apoanagyrus lopezi De Santis (Neuenschwander, 2001). While the practice of classical biological control has been questioned in recent years, due to the environmental risks posed by potential direct and indirect non-target
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impacts from the introduced natural enemies (Follett and Duan, 1999; Louda and Stiling, 2004; SimberloV and Stiling, 1996), Hoddle (2004) persuasively argues for the continued role of classical biological control in the Wght against the devastations caused by invasive pests. In this regard, the greatest challenges for biological control practitioners are to be able to identify and select the most eVective candidate control agents from the region of origin of invasive pests, and to minimize the likelihood of undesirable environmental impacts through eVective pre-release studies on the selected biological control agents. Thus in contrast to earlier biological control projects, emphasis in the future will be on minimizing the number of exotic species required to achieve successful biological control (McEvoy and Coombs, 1999), and maximizing the chances of successful suppression of the target pest. By the late 1980s it was evident that through the historical record of classical biological control there had been two extremes among the approaches used to select natural enemies as candidates for biological control introductions. At one extreme, an empirical approach (Ehler, 1990) sought to reconstruct the full natural enemy complex through the introduction of all suitable natural enemies form the region of origin. A good example of this approach has been the biological control program targeting the gypsy moth, Lymantria dispar L., in the northeastern United States, with more than 60 diVerent parasitoid and predator species released into the target environment (Dahlsten and Mills, 1999). The opposite extreme, often referred to as the holistic approach (Waage, 1990), attempted to identify the single best natural enemy species for introduction from the life history and behavioral characteristics of the natural enemies in relation to the demographic nature of the pest. This more theoretical approach to the selection of individual control agents is well exempliWed by the biological control program for the mango mealybug, Rastrococcus invadens Williams (Godfray and Waage, 1991). Here I will discuss codling moth, Cydia pomonella (L.), as a target for classical biological control, and the rationale that we have taken in selecting parasitoids for introduction into the western United States (California and Washington) for the classical biological control of this long-established invasive pest. Codling moth provides a valuable case study to illustrate some of the diYculties that a biological control practitioner faces in addressing the potential for success and the selection of candidate control agents.
2. Codling moth as a target for classical biological control Codling moth is a notorious fruit-boring pest that has extended its original distribution from the natural apple forests of Central Asia to cover all apple growing
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regions of the world, with the exception of eastern China and Japan. Recent interest in germplasm stocks from around the world, combined with the development of molecular markers, has demonstrated the ancestral role of Central Asia as the region of origin of the domestic apple (Geibel et al., 2000; Harris et al., 2002). While no comparable study has been made of the genetic structure of codling moth populations from around the world, it seems likely that the very close association of codling moth with apples would also point to Central Asia as a region of origin of this pest. In addition, although codling moth has frequently been recorded as a pest of pears, Asian pears, walnuts, and occasionally apricots, peaches, and plums (Barnes, 1991), it has only been recorded from these host plants in cultivated orchards. This suggests that it is the modern cultivars rather than the wild progenitors of these other tree crops that have been incorporated into the host plant range of codling moth as it expanded its distribution around the world. Codling moth Wrst appeared in the western United States in California in 1872 (Simpson, 1903), and has since become a devastating pest of apples causing almost complete crop loss in the absence of eVective management, and up to 40% loss of early-harvest pear cultivars and early-harvest walnut cultivars (Barnes, 1991; Mills, unpublished observations). As a potential target for classical biological control, the codling moth might be considered to rank very low in terms of the chances for success. One reason for this is that from the historical record of classical biological control introductions, as documented by the BIOCAT database (Greathead and Greathead, 1992), the rate of success for olethreutid moths has been particularly low in comparison with other families of pests (Fig. 1). In addition, as a fruit borer, codling moth is a direct pest that directly damages the harvestable part of the crop and thus even low densities of codling moth frequently
Fig. 1. The rate of success in classical biological control, estimated as the proportion of introduced parasitoid species that have resulted in partial to complete control of the target pest (using the single most optimistic outcome in cases of multiple records of introductions in diVerent regions), in relation to family of the pest (after Mills, 2000).
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exceed the economic injury level. From early on, Lloyd (1960a) recognized that direct pests have a far lower potential for success in classical biological control in comparison to indirect pests which can be tolerated more readily at low densities in the crop. Similarly, as a demand-side pest, feeding on fruiting structures that act as sinks rather than sources of photosynthate, the dynamics of codling moth populations might be expected to be little inXuenced by the action of natural enemies (Gutierrez, 1996). In contrast, one of the most valuable indicators of the potential for success in biological control is a much lower level of abundance of the target pest in its region of origin (Mills, 1990). Although codling moth is well known in Central Asia (Zlatanova, 1987), it is sporadic and far less abundant in natural apple forests, and also less abundant in orchards. This is in part due to the occurrence of only two generations per year in Central Asia in contrast to three generations per year in regions that have a longer growing season, such as California. Nonetheless, over a 4-year period of foreign exploration visits toward the end of the Wrst generation of codling moth in late June from 1996 to 1999, fruit damage in untreated experimental orchards in the region around Almaty in Kazakstan varied from 0 to 5% in comparison to 25–62% damage for the same generation in untreated organic orchards in California over the same time period (Mills, unpublished observations). While this diVerence in relative pest abundance between regions may have been due to a variety of factors unrelated to parasitism, in contrast to a situation of no diVerence in pest abundance between regions, it does not rule out a possible role for biological control. In addition, from an analysis of the biological control record, rates of success in the biological control of invasive insect pests have been greatest for exotic versus native plants, trees versus herbaceous plants, and cultivated versus natural ecosystems (Hawkins et al., 1999). Thus orchard crops, such as pome fruit and walnut orchards in the western United States, have good potential for success as they are characterized by exotic plants, supporting a reduced assemblage of insect herbivores in relation to native plants, cultivated ecosystems, with limited food web connectance and complexity in relation to natural ecosystems, and a tree crop environment, generating less disturbance than an annual row crop (Fig. 2). Finally, in any assessment of the suitability of an invasive pest as a target for classical biological control it is important to consider the economic value of the crops aVected by the pest and the potential for environmental beneWts from reduced use of insecticides. For the western region in 2002 apple production covered almost 200,000 acres generating an annual revenue of $1147 million, pears were grown on 69,000 acres with an annual revenue of $248 million, and walnuts were grown on 200,000 acres with an annual revenue of $305 million (Anon.,
Fig. 2. The rate of success in classical biological control (as deWned in Fig. 1) in relation to region of origin and architectural complexity of the crop plant, and degree of management of the ecosystem (after Hawkins et al., 1999).
2003). In addition, in 2001, damage suppression in apples and pears required from 1.8 to 6.4 and 1.5 to 2.0 applications of azinphos-methyl, respectively, whereas walnuts required 1.3 applications of chlorpyrifos (Anon., 2002). Thus codling moth is a key pest of fruit and nut production in the western U.S. both in terms of potential crop loss and insecticide usage.
3. Stage-structured model of codling moth population growth Codling moth, in common with other lepidopteran hosts, supports a rich assemblage of parasitoid species clustered into parasitoid guilds (sensu Mills, 1994a) that attack the host at successive stages in the life cycle and diVer in mode of development. What is the likelihood that a parasitoid that attacks a particular stage in the life cycle could provide suYcient suppression of codling moth populations to be successful as a biological control agent? Surprisingly, there have been few attempts to analyze the role of parasitism at diVerent stages in the life cycle of a pest in the suppression of pest population growth (but see Lin and Ives, 2003; Murdoch et al., 2003). Using a simple stage-structured model of parasitism of an aphid population, Lin and Ives (2003) found that as a result of removal of those individuals with the greatest reproductive value in the host population, parasitism of larger aphids caused a greater reduction in host population growth rate than parasitism of smaller aphids. Using a similar approach, we can assess the relative importance of parasitism at diVerent stages in the
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life cycle of codling moth through the development of a stage-structured population growth model. A stage-structured matrix model captures both the transition probabilities of individuals moving through the successive life stages, as determined by their respective development rates, and the survivorship of individuals within each stage. The matrix was parameterized for codling moth using fecundity and survivorship data for adults from Geier (1963) and Hagley (1972), egg development rate data from Geier (1963), larval, and cocoon development rate data from Setyobudi (1989), and egg, larval and cocoon survivorship data from Geier (1963) and Wearing (1975). The resultant projection matrix (Table 1) consists of a set of upper diagonal elements (Pi) representing the probability of an individual surviving and transitioning to the subsequent life stage, and a set of lower diagonal elements (Gi) representing the probability of an individual surviving and remaining in that life stage. These probabilities are dependent upon the survival (i) and the development (i) rates of each life stage (i) in relation to the time step of the projection (in this case 1 day), such that Pi D i (1 ¡ i) and Gi D ii. Finally, the top right element of the projection matrix represents the rate of fecundity (Fi), or more speciWcally, the product of the per capita oviposition rate per time step and the proportion of females in the adult stage. Following Caswell (2001), in the absence of parasitism, the projection matrix generates an intrinsic rate of increase for the codling moth population of r D 0.0272 and a population doubling time of 25.44 days. To assess the likelihood that parasitism occurring at a particular stage in the life cycle could be successful in the suppression of codling moth population growth, two diVerent approaches were taken; an analysis of the sensitivity of population growth to the stage-speciWc survivorship elements, and an analysis of the stage-speciWc rate of parasitism needed to reduce the intrinsic rate of increase to zero. The sensitivity of the codling moth model to its component vital rates is best analyzed through their corresponding elasticities, representing the proportional change in population growth that results from a
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proportional change in a particular vital rate. Elasticities depend not only on the reproductive value (vi) of individuals at that stage in the life cycle, but also on their rates of development (i) and survivorship (i). In a stage-structured model the elements of the projection matrix are the transition probabilities (Pi and Gi) for each stage, and the associated elasticities can readily be decomposed to estimate the contributions to population growth of both survivorship (i) and development (i) at each life stage (Caswell, 2001). The resultant elasticities for stage-speciWc survivorship indicate that, for the life stages that are susceptible to parasitism, the greatest responses occur in the Wfth instar and cocoon stages with some responsiveness also at the egg and second instar stages (Table 2). A corresponding analysis of the daily stage-speciWc rates of parasitism needed to reduce the intrinsic rate of increase of the codling moth population to zero shows a very similar pattern with 21.0 and 28.4% for Wfth instar and cocoon stages, and 34.6 and 36.3% for egg and second instar stages (Table 2). This analysis of the vulnerability of the codling moth life cycle to added parasitism provides two valuable insights. First, it suggests that codling moth population growth is most vulnerable to additional mortality at the Wfth instar or cocoon stage in its life cycle, and thus that parasitoids attacking these stages might be more Table 2 Analysis of the stage-structured population model for codling moth indicating the relative reproductive value (vi), the elasticities for survivorship (ei), and the daily percent parasitism required to achieve zero population growth (r D 0)
Egg L1 L2 L3 L4 L5 Cocoon Adpr Adr
vi
ei
Percent parasitism
0.016 0.024 0.049 0.060 0.067 0.072 0.150 0.269 0.293
0.073 0.034 0.067 0.036 0.021 0.101 0.151 0.032 0.185
34.6 47.8 36.3 48.4 59.2 28.4 21.0
Table 1 The projection matrix of the stage-structured population model for codling moth
Egg L1 L2 L3 L4 L5 Cocoon Adpr Adr
Egg
L1
L2
L3
L4
L5
Cocoon
Adpr
Adr
0.826 0.138 0.000 0.000 0.000 0.000 0.000 0.000 0.000
0.000 0.700 0.157 0.000 0.000 0.000 0.000 0.000 0.000
0.000 0.000 0.813 0.178 0.000 0.000 0.000 0.000 0.000
0.000 0.000 0.000 0.692 0.299 0.000 0.000 0.000 0.000
0.000 0.000 0.000 0.000 0.523 0.467 0.000 0.000 0.000
0.000 0.000 0.000 0.000 0.000 0.870 0.076 0.000 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.913 0.064 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.665 0.332
1.767 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.931
The elements in the upper diagonal are the probabilities of an individual transitioning from stage i to stage i + 1 (Pi), and the elements in the lower diagonal are the probabilities of an individual remaining in stage i (Gi) in the time step from t to t + 1. Life cycle stages include Li as larval instars, and Adpr and Adr as pre-reproductive and reproductive adults.
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eVective in the biological control of this pest than parasitoids attacking other life stages. Second, it also suggests that the egg and second instar stages could also be vulnerable to additional parasitism.
4. Comparison of parasitoid assemblages in North America and Eurasia Parasitoids of codling moth are readily collected by trapping larvae as they exit attacked fruit and descend the limbs to seek cocooning sites under the bark of the trunk. Parasitoid species reared from Weld collections of codling moth larvae and pupae trapped in 7.5 cm wide corrugated cardboard bands wrapped around the trunks and limbs of apple, pear, and walnut trees in a variety of organic or unsprayed orchards throughout California during the period 1992–2002 are shown in Fig. 3A. Also included in Fig. 3A is Trichogramma platneri Nagarkatti (Trichogrammatidae), an egg parasitoid that has been consistently reared from both naturally laid and experimentally expose codling moth eggs (Mills, 2003a). No attempt was made to collect parasitoids from larvae within fruit, and thus it is possible that we may have overlooked larval ectoparasitoids such as Eulophidae and Bethylidae. In contrast to an earlier survey of codling moth parasitoids in California (Lloyd, 1944), tachinid parasitoids were absent from our rearings, but Coccygomimus hesperus Townes (Ichneumonidae) was recorded as a true pupal
parasitoid. It is also notable that Ascogaster quadridentata Wesm. (Braconidae) was found only in apples, Macrocentrus ancylivorus Rowher (Braconidae) only in walnuts in the Central Valley, and Mastrus carpocapsae (Cushman) (Ichneumonidae) and C. hesperus were conWned to apple in coastal orchards. The only hyperparasitoid in the assemblage was Dibrachys cavus (Walker) (Pteromalidae), a Holarctic species that develops within the cocoons of primary parasitoids within the codling moth cocoon. The majority of these parasitoids are indigenous to California with the exception of A. quadridentata, a Palearctic species that was purposefully introduced into Washington state in the 1920s (Lloyd, 1960b). Codling moth has two generations per year in coastal California and three per year in the Central Valley. In general, levels of parasitism of codling moth were low and typically less than 5% in all areas (Mills, unpublished observations). However, egg parasitism by T. platneri frequently rose to 30–60% later in the season in unsprayed orchards, and parasitism of overwintering cocoons by M. carpocapsae was recorded to be as high at 23% in 1995 in one apple orchard on the Central Coast. The corresponding parasitoid assemblage in the Palearctic region (Fig. 3B) was investigated through trap banding of unsprayed apple trees in the regions around Changins in southwestern Switzerland and around Vienna in eastern Austria from 1992 to 1994, in the region around Almaty in southern Kazakstan from 1995 to 1998, and in the Illi Valley (Xinjiang Province) of
Fig. 3. The parasitoid assemblage associated with codling moth in (A) California, and (B) Eurasia. The circle represents the life cycle of the codling moth with YL, young instar larva; LL, late instar larva; and Coc, cocoon. The arrows represent the life stages attacked and killed by the associated parasitoids, those remaining outside of the circle being ectoparasitoids, and those passing through the circle being endoparasitoids.
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northwestern China from 1999 to 2003. Trapping in these surveys was primarily conWned to the Wrst generation of codling moth cocooning in June, with more limited sampling at the end of the season in each region. Although codling moth eggs were not sampled during these surveys for parasitoids of codling moth in Eurasia, it is well known that Trichogramma species do occur throughout the region (Dyadechko et al., 1975; Hassan, 1989; Zlatanova and Tarabaev, 1985), and thus a generic Trichogramma sp. has been added to Fig. 3B for completeness. Similarly, while no sampling of larvae within fruit was conducted during these surveys, Hyssopus pallidus (Askew) (Eulophidae) has been added to Fig. 3B, due to its known occurrence in France and Switzerland (Tschudi-Rein et al., 2004). Although most of the parasitoid species occurred on codling moth throughout the regions sampled, Bassus conspicuus (Wesm.) (Braconidae) and Trichomma enecator Rossi (Ichneumonidae) were found only in eastern Austria and southwestern Switzerland, A. quadridentata was absent from northwestern China, and Mastrus ridibundus (Grav.) (Ichneumonidae) occurred only in southern Kazakstan and northwestern China. In addition, although Bassus ruWpes (Nees) occurred both in Europe and Central Asia, it was much more consistent in the latter region. It should also be noted that the Liotryphon species found in Europe is L. caudatus (L.), while that found in Central Asia is a morphologically distinct but unidentiWed Liotryphon species. In addition to D. cavus, a second hyperparasitoid in the Eurasian parasitoid assemblage is Perilampus tristis Mayr (Perilampidae) that develops within the primary parasitoid larvae of A. quadridentata and B. ruWpes. These parasitoid assemblages are very similar to those recorded previously from Europe (e.g., Diaconu et al., 2000; Rosenberg, 1934; Simmonds, 1945), and for Central Asia (Durdyev, 1987; Zlatanova, 1987; Zlatanova and Tarabaev, 1985). One notable diVerence, however, was the presence of Pristomerus vulnerator Panz. (Ichneumonidae) in both southern Kazakstan and northwestern China, although it was absent in previous studies. Codling moth typically produces two generations per year in both the European and Central Asian regions
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that were surveyed in this study. However, the maximum levels of parasitism recorded from the trap bands in individual orchards diVered between the two regions. In Europe the highest rates of parasitism were recorded for A. quadridentata and P. vulnerator (Table 3). In contrast, in southern Kazakstan and northwestern China, both B. ruWpes and M. ridibundus were responsible for the greatest rates of parasitism.
5. Selecting eVective parasitoid species for introduction into the Western United States In response to concerns regarding the environmental risks of biological control, recent biological control projects have focused on host speciWcity as the main criterion for the selection of parasitoids for introduction. In addition to host speciWcity, which is directed toward minimizing the risk of non-target impacts, it is equally important to consider parasitoid eVectiveness and the potential to maximize the chances of successful suppression of the target pest. In view of this, we focus here on parasitoid eVectiveness, and the role of interactions and performance as indicators of success, rather than on host speciWcity, although the latter has also been addressed for this project (Unruh and Mills, unpublished observations). Our initial criteria for the selection of the most eVective parasitoid species for introduction into the western U.S. followed the guidelines suggested by Mills (1990). Of greatest concern was to select parasitoids that showed no evidence of antagonistic interactions. For this reason P. vulnerator was rejected, as it was known from an earlier project on the classical biological control of the European pine shoot moth Rhyacionia buoliana (Denis & SchiV.), that an unidentiWed Pristomerus species functioned as a cleptoparasitoid (Schroeder, 1974). As cleptoparasitism can be diYcult to recognize (Schroeder, 1974), and yet was considered to be one of the key reasons why Orgilus obscurator Nees was unable to successfully control European pine shoot moth in Canada (Dahlsten and Mills, 1999), the possibility of cleptoparasitism in the genus Pristomerus was considered suYcient reason to
Table 3 Maximum percent parasitism rates recorded in individual orchards (with sample sizes of greater than 60 host individuals) for the primary parasitoids collected from banding apple trees in Europe (western Switzerland and eastern Austria) and Central Asia (southern Kazakstan and northwestern China, Xinjiang Province) Europe
Ascogaster quadridentata Bassus conspicuus Bassus ruWpes Pristomerus vulnerator Trichomma enecator Liotryphon spp. Mastrus ridibundus
Central Asia
Switzerland 1992–1993
Austria 1992–1994
Kazakstan 1995–1998
Xinjiang 1999–2003
10.3 — 0.7 32.4 9.9 1.5 —
42.6 3.2 — 27.9 7.4 1.4 —
14.5 — 33.3 3.1 — 3.7 43.9
— — 13.6 0.6 — 4.1 1.4
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reject P. vulnerator despite the fact that it remains unknown whether this particular species is cleptoparasitic within the codling moth parasitoid assemblage. As a larval ectoparasitoid, H. pallidus exhibits rapid larval development (Zaviezo and Mills, 1999) which conveys a competitive advantage through a priority eVect over larval endoparasitoids that show protracted larval development (see Mills, 2003b, for further details of parasitoid interactions). As there is some evidence from the literature that lepidopteran parasitoid assemblages that include a greater species richness of larval ectoparasitoids show a reduced richness of larval endoparasitoids (Mills, 1994b), H. pallidus was also considered a potential antagonist. From a more detailed analysis of the interaction of H. pallidus and A. quadridentata it was shown that not only does H. pallidus have competitive superiority, but also that it experiences a distinct Wtness advantage from parasitizing host larvae previously parasitized by A. quadridentata (Zaviezo and Mills, 2001). The Wtness gain by H. pallidus from multiparasitism was considered functionally similar to cleptoparasitism (Mills, 2003b) and suYcient reason to reject this species from consideration as a biological control agent for codling moth. Additional criteria used in the selection of eVective candidates from the Eurasian parasitoid assemblage of codling moth were level of parasitism, and vulnerability of the codling moth life cycle (see Section 3). Hawkins and Cornell (1994) have shown that the likelihood of success in classical biological control is directly related to the extent of parasitism that occurs in the region of origin, with a threshold for success of approximately 30% parasitism. In addition, the earlier analysis of a stage-structured model for codling moth suggested the greater vulnerability of population growth to additional mortality in the second instar and cocoon stages. Using these combined criteria, the larval endoparasitoid B. ruWpes, and the two prepupal ectoparasitoids Liotryphon spp. and M. ridibundus were selected for further consideration. B. ruWpes was recognized as an important parasitoid of codling moth in Kazakstan by Zlatanova (1970) and was the only young larval parasitoid to achieve suYcient levels of parasitism in the surveys conducted in Central Asia (Table 3). Although only one of the two prepupal parasitoids, M. ridibundus, was also dominant in terms of levels of parasitism observed from surveys in Central Asia (Table 3), both were selected as they attack the vulnerable cocoon stage in the life cycle. As cocoon parasitoids, Liotryphon spp. and M. ridibundus could act as facultative hyperparasitoids of primary parasitoid cocoons, such as those of B. ruWpes and A. quadridentata. However, in no-choice tests, neither L. caudatus nor M. ridibundus showed evidence of facultative hyperparasitism (Unruh and Mills, unpublished observations). In view of these results, B. ruWpes, L. caudatus, and M. ridibundus were considered potential candidates for introduction into the western U.S.
A variety of additional traits have been suggested as potential criteria for selection of the ‘best’ parasitoid species for biological control introductions (HuVaker et al., 1977; Kimberling, 2004; May and Hassell, 1988; Murdoch et al., 2003). As summarized by Murdoch et al. (2003), from a theoretical perspective, all else being equal, desirable parasitoid attributes include a higher rate of successful search, a shorter generation time, a preference for patches of higher host density, an absence of host refuges, a preference for host stages of longer duration or that suVer less background mortality, and a greater number of female oVspring produced per attacked host. However, it is clear that trade-oVs have occurred in the evolution of parasitoid life history traits, and that any particular trait may be accompanied by a suite of others that may be less desirable. As a result this reductionist approach has led to few, if any, general principles to guide the selection of the ‘best’ parasitoid species for introduction. Nonetheless, it is worth noting that of the three parasitoids selected above as potential candidates for introduction against codling moth, M. ridibundus exhibits the greatest range of desirable attributes. These include a positive response to patches of higher host density (Bezemer and Mills, 2001), a shorter generation time than its host, allowing it to complete at least two generations on diapausing cocoons of codling moth in the fall (Mills et al., 2004), and gregarious development with the production of an average of 2.4 females per attacked host (Bezemer and Mills, 2003).
6. Conclusions Although considered a target for classical biological control both in the 1920s and again in the early 1960s (Lloyd, 1960b), codling moth has been ignored more recently by biological control practitioners due to the fact that it is a direct pest. As a result codling moth remains a key pest of fruit and nut production in the western U.S. causing substantial crop losses and necessitating continued reliance on within-season insecticide applications to achieve adequate control. A need to reduce insecticide residues in fruit crops (e.g., Melnico, 1999; Smith, 2001) prompted this more detailed analysis of the potential for biological control of codling moth and the selection of parasitoid species for importation from Central Asia. Our analysis focused on orchards as a suitable environment for biological control success, the lower level of abundance of the pest in its region of origin, and the selection of parasitoid species that both avoid the potential for antagonistic interactions and target the vulnerable second instar and cocoon stages of the life cycle. As a result of this approach, the three parasitoids B. ruWpes, L. caudatus, and M. ridibundus were imported
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and released at numerous locations in both California and Washington (Unruh and Mills, unpublished observations). The outcome of these releases is that B. ruWpes has yet to be recovered, L. caudatus has at least temporarily established in California, and M. ridibundus has been recovered from numerous sites in both states and appears to be well established. Codling moth damage in walnuts in California has declined since the release of M. ridibundus in 1996 with parasitism of overwintering cocoons reaching 70% in some unsprayed orchards (Mills, unpublished observations). The outcome of the project cannot be considered a dramatic success, as should be expected in the case of a direct pest (Lloyd, 1960a), but as noted by Goldson et al. (1994), the value of parasitism and the contribution of partial biological control to the overall management of such notorious and intractable pests as the codling moth should not be underestimated. Thus codling moth as a case study in the selection of parasitoid species for introduction in a biological control program for an invasive pest, suggests that there is considerable merit in the use of a more holistic approach. First, a suYcient understanding of the dynamics of the target pest population can be informative in identifying the most vulnerable life stages. Second, a suYcient understanding of the biology of the parasitoids occurring in the region of origin of a target pest is necessary to avoid the potential for antagonistic interactions among selected parasitoid species, particularly when the pest is holometabolous and supports a more complex parasitoid assemblage. A more recent theoretical analysis has further suggested the importance of niche overlap in selecting eVective parasitoids for introduction (Pedersen and Mills, 2004). The occurrence of spatial, temporal or behavioral refuges from parasitism can allow individuals in a pest population to escape from attack by an introduced parasitoid. Consequently, the identiWcation of an additional parasitoid species that can break the host refuge from parasitism provides a powerful opportunity to achieve greater success in biological control. Thus, although biological control has been considered more of an art than a science, the development of a stronger scientiWc basis for the selection of eVective parasitoids for introduction can be used to maximize the potential impact of parasitism for those intractable target pest groups, such as fruit pests, that have historically shown low rates of success in biological control.
Acknowledgments Funding for this project was provided by the Walnut Marketing Board and the Pear Research Advisory Board of California, and the National Research Initiative of the USDA CSREES, Grant No. 0012862.
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