Copyright 1976. All rights reserved

BIONOMICS AND -:-6109 MANAGEMENTOFRHAGOLET�

E. F. Boller Swiss Federal Research Station for Arboriculture. Horticulture. and Viticulture. CH-8820 W1idenswil. Switzerland

R. J Prokopy Prokopy Bio-Experimental Farm. Bailey's Harbor, Wisconsin 542021

INTRODUCTION

Characteristics 0/ Rhagoletis

The genus Rhagoletis, of the dipteran family Tephritidae, includes some 50 de­ scribed species and is widely distributed over the Holarctic and Neotropical regions (I, 41, 66, 171, 178). The larvae of all known Rhagoletis feed in the pulp of developing fruit, and several species are important economic pests (191). Occasion­ ally, a Rhagoletis species may be regarded as potentially beneficial, as when R. a/temata was assessed for release as an agent in the biological control of Rosa rubiginosa. a harmful weed in New Zealand (63). Unlike the multivoltine and largely polyphagous species of the economically by U.S. Department of Agriculture on 12/09/10. For personal use only. important genera Dacus, Anastrepha , and Ceratitis, most Rhago/etis species are univoltine and oligophagous. Some of them (e.g. pomonella, cingulata , fausta , in­ Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org dijferens, lycopersella ) have shifted from their economically unimportant native hosts, and established new races on introduced cultivated plants during the past century.

The L iterature

Since 1960, various aspects of the biology or control of most North American Rhagoletis species have been reviewed by Christenson & Foote (5 1), Bush (41 --45), Dean & Chapman (59), Bateman (17), and Rivard (169). Comprehensive bibliogra­ phies have been published on pomonel/a (169) and on cingula ta , indijferens, and

IAfter September I, 1975, Dr. Prokopy's address will be Department of Entomology, University of Massachusetts, Amherst, Massachusetts 01002.

223 224 BOLLER & PROKOPY

ja us ta (6). No recent bibliography exists for completa, but for ce ras i the European literature up to 1933 has been covered by Thiem (185). A comprehensive bibliogra­ phy on ce rasi is in preparation (A. Haisch, personal communication). Published studies on Rhagoletis have focused almost exclusively on those species of economic importance. Two species have received the most attention: The North American apple maggot,po monella, which attacks apples and also, in some locali­ ties, cherries, plums, apricots and pears, and the European cherry fruit fly, cerasi, which attacks sweet and sour cherries. Other economic pests receiving significant but lesser attention include the North American species cingu la ta, indijferens, and fausta , which attack sweet and sour cherries, mendax, which attacks blueberries, completa and sua vis, which attack walnut and in some localities peaches, and bas iola, which attacks rose hips; the European species alfe ma ta , which attacks rose hips; and the South American species Iycopersella, which attacks tomatoes. This review is based in general on the published information on these 11 species. With some notable exceptions, the bulk of investigation on Rhagoletis has re­ flected the historical development of pest control concepts and has until recently been concerned primarily with control by insecticides and with those aspects of Rhagoletis biology most relevant to achieving such control. Certain aspects of biology vital to the development of integrated control procedures are still poorly understood and will require special attention in the future. In this review, we attempt to provide a balanced discussion of Rhago/etis research principally carried out in Europe and North America. We focus mainly on new knowledge gained during the past decade or so, evaluate this knowledge, and try to point out some existing problems and potential avenues of research. We examine first the biology of individuals, then that of popUlations, and lastly, management.

BIOLOGY OF INDIVIDUALS Eclosion Rhagole tis adults emerge from puparia beneath the larval host plant. This process occurs primarily in the morning hours (11, 36, 59, 67, 98), and in basiola is by U.S. Department of Agriculture on 12/09/10. For personal use only. stimulated by rising morning temperatures (11). The flies, which are capable of flight and feeding within two hours of emergence (36, 98,138, 192),evidently spend little Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org time on the ground or understory vegetation before leaving (119). Females emerge usually earlier in the year than males, and the sexes reach equilibrium at peak emergence (7,73, 172,180). Pomonella flies from pupae that remai�ed in diapause for two years emerged 1-2 weeks later than the normal population, as did flies from pupae that developed from late apple varieties (7, 137, 142). Synchronization of fly emergence patterns with the ripening pattern of host fruit has been demonstrated in cerasi and proven a valuable aid in differentiating host races (28). Adult Feeding Food is required for gonadal maturation, which in most Rhagoletis species occurs within two weeks of emergence. The flies'search for food is not confinedto the larval BIONOMICS AND MANAGEMENT OF RHAGOLETIS 225

host plant and may carry them to various types of neighboring vegetation (124, i 92). Evidence is accumulating that the principal food source is insect honeydew (34,77, 111, 131; V. Vallo, personal communication) and that probable additional food sources are plant liquids exuding from glandular structures, wounds, and oviposi­ tion stings (36, 47, 61, 102, 192), numerous bacteria (59), yeasts and fungal spores (36), and insect frass and bird dung. Contact chemoreceptors for food detection have been described in pomonella (l11) and cin gula ta (68). Early workers established that ingestion of water and carbohydrate enhances longevity. But not until Fluke & Allen (65) supplied captive pomon ella flies with yeast was it known that proteinaceous or amino nitrogen was necessary for repro­ duction. Further definition of the nutritional requirements of adult Rhagoletis (36, 55, 93) eventually led to the development of chemically defined diets for pomonella (34, 128) and completa (189). The knowledge that insect honeydews are usually deficient in certain essential amino acids and probably also in other important nutrients led to the suspicion that the missing nutrients are provided by symbiotes (34, 78) in many fruit .flies (17). Indeed, Pseudomonas me/ophthora, the bacterial symbiote associated with pomo­ nella (8, 10), has been shown capable of synthesizing 18 amino acids (113) and degrading unsuitable food components, including;nsecticides (35). Symbiotes have received increased attention recently in comp/eta (189), cerasi, a/temata , and meigen i (71, 83). No one has studied the quantity of food required by Rhago/etis for normal fecundity. A paucity of honeydew on vegetation supporting large reproducing Rha­ go/etis populations has often been observed (59). In view of Fytizas' findingthat one day's exposure of Dacu s oleae females to protein hydrolysate was enough to support a high level of reproductivity over the next 14 days (69), we speculate that the quantity required by Rhagoletis may be less than previously assumed. Dispersal As pointed out by Bateman (17), two types of movement are discernible in adult fruit flies: dispersive and nondispersive movement. The latter is typical of Rha goletis

by U.S. Department of Agriculture on 12/09/10. For personal use only. under normal crop conditions; activities associated with feeding, mating, and oviposition rarely take individuals very far from their host plants. Such restricted

Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org movements have been reported frequently in Rhago/etis species such as comp/eta (15, 36), in differens (67, 90, 143), pomonella (39, 124, 140, 142), and cerasi (30. 195). Dispersive flights have been observed in completa (15), cerasi, (31, 112, 172) and pomonella (108), mostly in situations in which flies were deprived of suitable fruit for oviposition because the crop was destroyed by frost or early harvest. Flight studies in the laboratory with cerasi (168) have shown that flies are capable of flying several kilometers in 24 hr on rotating arms if they are deprived of landing plat­ forms-distances apparently never flown in nature. These data indicate, however, that natural barriers that provide isolation in genetic control programs, such as forests or open fields without attractive silhouettes, might become less effective in seasons when crop failures induce dispersive movements. 226 BOLLER & PROKOPY

Host Detection

With approaching sexual maturity, flies move to larval host plants, the site of assembly for mating (41, 43, 158) and oviposition. Mature flies of both sexes accu­ mulate in greatest numbers on hosts bearing large crops of fruits in prime stage for oviposition (30, 108, 124, 147, 163, 164, 192). Except for recent studies on pomonel/a, the process of host-plant detection by Rhagoletis flies has received scant attention. Foliage color, tree shape, and tree size all play a role in eliciting fly arrival in this species, but none of these cues seem specificto host plants (115). The odor of susceptible host fruit, however, is a specific stimulus that attracts (or arrests) the flies (163). A host-specificleaf stimulus acting as contact arrestant also appears to play a role in host recognition in pomonella (43) and cerasi (E. F. Boller, unpublished data). After arrival on the host plant, the flies detect the fruit solely on the basis of its physical characteristics of shape, contrast-color against the background, and proba­ bly size (52, 147, 149, 196). Few flights to fruit are made by immature flies (38, 52, 159, 196), or mature flies under conditions unfavorable for mating or oviposition (159). Movement of both mated and unmated Rhagoletis females onto fruit is believed to be motivated primarily by ovipositional drive (4, 36, 161; B. Katsoyan­ nos, in preparation). Male Rhago ietis establish territories on the fruit and defend them aggressively (4, 36, 38; E. F. Boller, unpublished data) while waiting for females. Males of pomonella and cerasi are arrested on the fruit by pheromones deposited principally by females (160; B. Katsoyannos, unpublished manuscript), thereby enhancing the probability of encountering a mate in the vicinity.

Mating

Mating in all Rhagoleti s studied to date is initiated on or near the host fruit (4, 36, 38, 41, 158). The confinement of mating to the host plant appears important for insuring precopulatory reproductive isolation in several species (41, 43, 161). For example, when pomonel/a shifted recently to sour cherry as a new host, neither sex

by U.S. Department of Agriculture on 12/09/10. For personal use only. was readily able to distinguish its own species from the already present fau sta, and numerous interspecific matings were observed (161).

Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org The visual stimulus of a female or male moving on the same fruit or nearby elicits the attention of waiting males. Mounting is achieved by a jump or short flight onto the female's abdomen; females engaged in some phase of oviposition behavior are often particularly receptive and provide strong stimuli for male pursuit (36,38,41; 161). Male pomonella (152) and cerasi (B. Katsoyannos, in preparation) secrete a pheromone that in high concentration and over short distance attracts virgin females. In natural concentration it is hypothesized to function primarily as an aphrodisiac. No other attractive sex pheromone nor any acoustical signals have been observed in Rhagoleti s. Mating behavior in Rhagoletis is comparatively easy to study because it is lo­ calized, diurnal (36, 159), and frequent (II, 36, 67, 88, 112) in order to insure high egg fertility (22, 127). Thus, we anticipate that research in this area will increase. BIONOMICS AND MANAGEMENT OF RHAGOLETIS 227

OViposition Rhagoletis flies oviposit into growing fruit, rarely or never into fallen fruit (138) except under laboratory conditions. Two facts suggest that the stimuli eliciting oviposition are not necessarily specificto host plants suitable for larval development: (a) in nature (72, 123) as well as in the laboratory (36, 81, 195) , some Rhagoletis are known to deposit eggs into fruit in which the larvae cannot survive, and (b) artificial oviposition devices devoid of host material can elicit a high degree of oviposition (24, 145, 156, 189). Nonetheless, it is true that shape, size, color, surface structure and condition, and chemistry of a fruit all may play a role in eliciting oviposition (52, 59, 70, 145, 156, 162, 196). Ovipositor penetration into the fruit depends on skin thickness and skin or flesh hardness (11, 36, 145, 156, 196). Whether an egg is deposited depends on sweetness and moistness of the fruit interior in completa (52, 189), on light conditions in cerasi (22), and probably on many other unidentified factors in all species. Oviposition is diurnal, and environmental conditions influence the number of eggs laid (22, 36, 159) and the location of the punctures on individual fruits (11, 22,36, 82, 185). Fecundity of most species is about 300--400 eggs per female under optimal conditions. Rhagoleti s deposit usually only one egg per clutch. Exceptions are some of the walnut infesting species, which lay IS or more eggs at a time (3 6, 58). Of particular interest in Rhagoleti s oviposition behavior is the dragging of the ovipositor around the fruit surface after egg deposition. In the four species studied to date (p omonella, completa, fau sta, and cerasi), a marking pheromone that deters repeated ovipositions into the same fruit is deposited on the fruit surface during ovipositor dragging (52, 150, 153; B. Katsoyannos, unpublished manuscript). Oviposition-deterring marking pheromones are common among entomophagous parasites, but Rhagoleti s represent the only known cases among plant parasitic insects. Rhagoleti s have a definite tendency toward uniformity in egg dispersion among available fruits (48, 76, 154). Marking pheromones, along with aggressive encounters between females (4, 20), are apparently the principal means for mediat­ ing this egg dispersion and the consequent full exploitation of available host fruits for larval development. Large glands emptying into the vagina (36, 54) possibly by U.S. Department of Agriculture on 12/09/10. For personal use only. serve as sites of pheromone production or storage. Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org Larval Development

Rhagoleti s eggs hatch within a few days of oviposition. With rare exceptions (110), larvae confine their feeding in general to the same fruit in which the eggs were laid. Larval survival in the fruit may approach 100%, and development may be com­ pleted in about two weeks if the fruit is soft (11, 23, 59, 94, 186). Sugar content and acidity of the fruit flesh influence larval growth rate (23, 59). Symbiotes, transferred by adults to eggs and host tissue, play apparently an important role in larval nutrition (8, 78, 83, 113, 189). The larvae of pomonella (125, 14 6) , cerasi (31, 79), and co mp leta (K. S. Hagen, personal communication) can be reared on artificial media, but chemically defined larval diets have not been established for any Rhagoletis. 228 BOLLER & PROKOPY

Mature larvae (95) bore emergence holes through the fruit's skin and drop to the ground early in the morning (23, 36, 138, 142), with increasing morning temperature apparently being the main stimulus in cerasi (23). They burrow into the soil to a depth of usual\y not more than 10 cm (36, 67, 98, 106, 138, 192) and pupate within a few days (36, 179). Pupating larvae are highly subject to desiccation (36, 87) and predation (23, 26), especially by ants.

Pupa and Diapause ' Developments associated with the pupae have received a good deal of attention by Rha goletis workers as this stage is the longest to be exposed to the environment. Most pupae of temperate Rhagoletis undergo a winter diapause that is normally completed after pupal exposure to low temperatures. Development continues in spring when temperatures increase (102, 121, 175, 183, 199), with moisture level also a factor (18, 122, 194).1 In some cases, conditions may be insufficient for diapause termination in all pupae the first spring, and some may remain in the soil for two or even up to five winters before producing adults (II, 36, 98, 109, 137, 184, 192). Such pupal carryover is a highly adaptive trait in insuring that the population will not perish on account of failure of hosts plants to fruit in some years. This phenome­ non is important in the proper planning of control programs that aim at a total elimination of the target species in a given area (see s�ction on management). The Neotropical species lycopersella is different from all other Rhagoletis studied in that its habitat is extremely dry, with estivation of some pupae being terminated by exposure to moisture (178). Fractions of the pomonella , in differens, and cerasi populations and most puape of lycopersella , rather than undergoing diapause, may instead give rise to a new generation of adults within a few weeks of pupation (67, 87, 178; K. Russ & E. F. Boller, unpublished data). The larval progeny of second-generation pomonella flies are in most cases probably unable to complete development before succumbing to low winter temperature (50); however, they are apparently able to do so in the southern part of their range (62). Diapause induction in pomonella is regulated by photoperiod acting on the larvae

by U.S. Department of Agriculture on 12/09/10. For personal use only. and by temperature acting on larvae and pupae (148). There may be little or no incidence of diapause under long-day-high-temperature conditions, whereas short

Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org photoperiod coupled with low temperature results in total diapause. Conditions in between give rise to a few nondiapausing individuals, which have been selected as progenitors of a nondiapausing strain (9). Diapause in some cerasi and comp/eta pupae has been prevented or terminated by application of chemicals (104, 199) or by soaking pupae in water immediately after pupation (199). The mechanisms of diapause regulation in Rhago/etis are not yet fully understood.

Longevity Fly longevity in nature has never been established accurately for any Rhago/etis species. Estimates of average longevitty range from two weeks for cerasi (based on recapture of marked flies) (E. F. Boller, unpublished data), three weeks for mendax BIONOMICS AND MANAGEMENT OF RHAGOLETIS 229

(98), and three to six weeks for completa (36) and pomonella (46, 56). Temperature, humidity, and light are known to influence longevity, which is greatest in cool weather (36, 67, 93).

BIOLOGY OF POPULAnONS

Population Dynamics Ecological information on Rhagoletis is abundant in the literature and varies from thorough investigations to anecdotal observations in the field. Many aspects have been reviewed recently by Bateman (17). Regional histories of population fluctua­ tions have been reported for pomonella (59, 170), cerasi (29, 102), and North American cherry fruit flies (cf 6). It was not until the early 1960s, however, that Rhagoietis populations were analyzed systematically in comprehensive studies.

LIFE TABLES The first partial life table in Rhagoietis, published in Canada for pomonella in 1963 (100),adopted the classical Canadian sampling techniques devel­ oped for orchard pests (101). Although no key factors were determined and mortal­ ity was assessed only in the egg and larval stages, it became evident that predators played a significant role in the 80% mortality of the larval population. Sampling techniques for pomonella were refined further by Cameron & Morrison (48), allow­ ing for the firsttime a quantitative analysis of the regulating processes. Low mortal­ ity occurred during the egg stage but reached high levels in larvae and pupae, with pupal mortality suspected of having a regulatory function in Quebec (26, 48). Comprehensive ecological studies were carried out on the same species in Nova Scotia, and data await final analysis (W. T. A. Neilson, personal communication). The firstsemiquantitative life table, which was published in 1966 for cerasi. showed that predators were the predominant mortality factors in the larval. pupal. and adult stage (23). However, prevailing weather conditions during the short oviposition period of the pest were considered crucial for the regulation of population densities. This view was supported by observations in Poland (102). It was concluded that natural mortality factors alone were not effective enough to reduce the populations

by U.S. Department of Agriculture on 12/09/10. For personal use only. below the economic thresholds set by the market (23. 26. 105). Regulating factors such as weather. time of fruit ripening. crop size •• and varietal susceptibility have Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org been described in indifferens (67), completa (36). mendax (98), pomonella (37,46, 59). and cerasi (102, 112. 192). Whereas these factors exert a great influence on the reproductive potential of Rhagoletis. biotic mortality agents acting in the soil seem to play an important part in destroying significant amounts of pupae, the extremely long pupal stage of the univoltine Rhagoietis often being the crucial period of the entire life cycle during which high mortality occurs (26).

BIOTIC MORTALITY FACTORS Parasites of Rhagoletis received the attention of early workers as their occurrence is more conspicuous than that of predators. A list of parasites attacking cerasi was published recently by specialists of the Common­ wealth Institute for Biological Control in their search for potential enemies of North 230 BOLLER & PROKOPY

American Rha goletis spp. (3, 49). The pupal parasite Ph ygadeuon wiesmanni is most effective (23, 49, 192), causing up to SO% pupal mortality in northwest Switzerland (23). Larval parasites occur in higher numbers in eastern Europe (102, IS4; V. Vallo, personal communication), but their effectiveness is greatly impaired by their short ovipositor, which can not reach cera si larvae in large cultivated cherries (l12). Similar observations on Rha goletis parasites, which are more numer­ ous on the smaller wild host fruits than on cultivated varieties, have been reported for indifJerens (67) and cinguiata, fausta, and pomonella (l11). The status of parasites in pomonella has been reviewed recently by Monteith (l18) and confirms earlier reports (111) that parasites play a minor role in commercial orchards. How­ ever, they might be useful in reducing pomonella populations in wild and neglected trees (11S). R. comp/eta has been described as being remarkably free from important natural enemies, especially parasites (36). Because earlier workers focused mainly on parasites, information on predators is scarce and consists mostly of anecdotal reports or occasional observations (36, 37, 46, 47, 9S, 100, 142, IS4, 192). This situation was recognized in 1965 by the International Biological Programme (IBP) group working on fruit flies, and empha­ sis was put on a coordinated international research program to study predators that act on the pupae in the soil (26). Studies on six tephritid species, including two Rha goletis species, were carried out simultaneously. Data obtained on cerasi (Swit­ zerland and eastern Czechoslovakia) and pomon ella (Canada) not only confirmed earlier reports (23) on the impact of predators on Rha goletis pupae but also yielded new information on time, location, and body size of predators acting in the soil (26). The main pupal predators in pom on ella were crickets (117), ants, and carabids (I. Rivard, personal communication). The status of predators of adults was reviewed by Monteith (119). Feeding tests and serological analysis carried out on cerasi showed that ants, unlike 'carabids, staphylinids, or myriapods, could not detect andlor crack the puparia. At deeper soil strata, cerasi pupae were destroyed by small, unidentified organisms believed to be mites (23, 26). Ants, however, were important predators of cera si larvae dropping from the fruit, as well as of emerging adults (23). It is noteworthy that predators may act at higher levels of the food chain

by U.S. Department of Agriculture on 12/09/10. For personal use only. than parasites and hence destroy parasites that have previously killed the prey (23, 26, liS). Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org Population Genetics and Speciation

GENETIC VARIATION BETWEEN POPULATIONS Within the same species, North American Rhagoletis tend toward an overall reduction in size at the southern limits of distribution (41). A recent analysis of cerasi collected throughout its range in Europe has revealed that major differences exist between various geographically defined populations. Emergence patterns observed in 27 population samples indicated a short concen­ trated emergence period in Central European populations, which became extended with decreasing latitude and increasing altitude. The apparent synchronization of fly emergence with the ripening period of cherries and wild hosts suggests that cerasi BIONOMICS AND MANAGEMENT OF RHAGOLETIS 231

does not consist of one homogeneous interbreeding European population but rather is composed of a complex of populations or races, each with its own biological characteristics (28). Some of the flies sampled were utilized in hybrid crosses. The observed sterility of eggs produced by the cross between Swiss males and Turkish females triggered a systematic hybridization program carried out simultaneously in Switzerland, Austria, Czechoslovakia, and Germany that yielded unexpected re­ sults. R. cerasi populations form two complexes that exhibit a high degree of unidirectional incompatibility (27, 28). This discovery stimulated new investigations on ce rasi on national and international levels (27) to deal with the definition of dividing lines between the complexes (E. F. Boller and co-workers, in preparation; K. Russ and co-workers, in preparation), the mechanisms of incompatibility (27), and ecological and behavioral characteristics of the individual populations. Al­ though the practical implications of these phenomena on future control strategies against ce rasi can not be assessed yet, it is evident that the research in progress will increase our basic knowledge of this important pest and strengthen the existing collaboration among Rhagoletis workers. It is anticipated that similar investigations will be carried out in North America on Rhagoletis; the comparative analysis of allozymes and other proteins has already received advanced attention (45, 176, 177). Here is a unique opportunity for collaboration between applied and basic research­ ers that could speed up the transformation of basic biological knowledge to valuable input at the grower's level.

Wild and la boratory populations The pitfalls of mass-rearing techniques for insects that are to be used as carriers of lethal features to their wild counterparts in the field and the danger of reduced quality of laboratory-adapted ecotypes have recently received increased attention (25). The advanced sterile insect technique (SIT) pro­ grams for control of cerasi in Europe (see section on management) have made the European cherry fruit fly the model Rhagoletis species for the development of quality control concepts and techniques. Methods for monitoring flight characteris­ tics (168), mating activity (32), and host recognition (B. Katsoyannos, personal communication) have been developed or adapted for application in ce rasi, and by U.S. Department of Agriculture on 12/09/10. For personal use only. systems for monitoring the degree of genetic variation at the enzyme level are being developed for this species. Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org

HOST RACES AND SPECIATION The origin and evolution of species and host races in phytophagous insects have long been a source of disagreement among evolutionary biologists. The difficulty in resolving whether new host races and species arise sympatrically or whether geographic isolation is a prerequisite for speciation in all sexually reproducing animals stems from a paucity of detailed studies of wild insects. Existing information has been derived primarily from studies on a few economically important phytophagous pests. One such group that has received particular attention is the genus Rhagoleti s. The abundant literature on this subject has been reviewed recently by Porter (143), Christenson & Foote (51), Bush (41, 43), and Simon (176), but these authors covered Rhagoletis only in North America. 232 BOLLER & PROKOPY

Cherry fruit flies in Europe and North America are still the object of controversy, begun decades ago, over the status of races attacking cultivated and wild hosts (13, 185-187, 195). R. ce rasi, mentioned already in 1540 as a pest of cherries, was observed in 1840 infesting the indigenous honey-suckle Lonicera xylosteum (185) and also attacking the recently introduced L. tatarica frequently found in parks. Some 40 years ago, Thiem in Germany and Wiesmann in Switzerland investigated in detail the host situation in ce rasi and began a controversy over their conflicting conclusions as to the practical importance of Lonicera as a source of infestation for cultivated cherries (187, 192). Both claimed that the cherry- and honeysuckle­ infesting forms were identical on morphological grounds, but Thiem considered Lon icera shrubs as major breeding ground for cerasi and postulated an eradication program for Lonicera in the cherry-producing areas of the German empire (185). However, Wiesmann (195) observed differences in the emergence patterns of flies reared from the two different hosts, which indicates adaptation of the flies to the ripening periods of their hosts and a possible beginning of host-race formation. His conclusions were confirmed in recent investigations (28). The status of cerasi. re­ ported to infest Be rberis vulga ris in eastern Europe (92) and later described as new species (89), was ascertained on the basis of differential emergence patterns (28) and gene-frequencies (G. L. Bush and E. F. Boller, in preparation). A situation similar to that in cerasi occurs in in differens (13) in North America, and it is anticipated that future research will lead to the clarification of the intriguing host-races prob­ lems.

MANAGEMENT

The development of concepts and methods for control of injurious Rhagoletis species reflects the history of insect control in general. Early methods focused on destruction of infested fruit were followed by the eras of inorganic insecticides and the advent of organic pesticides. which led to the insecticide boom of the 1950s and early 1960s. In recent years, there has been a growing search for more broadly based approaches to Rhagoletis management in the framework of integrated control; this by U.S. Department of Agriculture on 12/09/10. For personal use only. topic was recently reviewed by Hoyt & Burts (86).

Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org Economic Thresholds The economic threshold of Rhagoletis attacking commercial fruits is low, inasmuch . as the progeny of a single female may infest some 200 or more fruits. While consumer intolerance of fruit injury has reached the point of being unreasonable, undamaged fruit nevertheless brings the highest prices, and tolerance limits are as low as 4% infestation of cerasi and pomonella larvae in fruit for table and canning use (29, 130). There is no tolerance of pomonella infestation of apples for exporta­ tion (50. 130) in either the United States or Canada. Complete larval mortality occurs when infested fruit is stored under cold (50) or controlled atmosphere condi­ tions (74), or is fumigated (173), which alleviates this particular problem. The low tolerance has been the principal reason for the extensive use of preventative-type insecticide applications against Rhagoletis and is the major barrier to application of alternative control methods. BIONOMICS AND MANAGEMENT OF RHAGOLETIS 233

Forecast and Sampling

Techniques for sampling Rhago/etis populations have been aimed largely at deter­ mining the time of appearance of the earliest-emerging flies of the season, and the current widespread recommendation is to apply insecticides at that time. These techniques have included (a) using fly emergence cages placed under infested host plants (36, 46, 47, 98, 185) or checking the development of planted pupae (174, 184); (b) forecasting emergence on the basis of host plant phenology (97), field tempera­ ture summation data (36, 64, 91, 97, 188), or, in cerasi-with a high degree of accuracy-soil temperature summation data in conjunction with temperature thresholds for pupal development (21, 102, 120); and (c) monitoring firstfly appear­ ance by using traps. Knowledge of first fly appearance may be important to proper timing of insecti­ cide application against species exhibiting a short emergence and preoviposition period, such as cerasi. But the usefulness of this approach is doubtful in such species as pomonella and completa, which have longer emergence and preoviposition peri­ ods. Inconsistent emergence patterns of earliest flies is common in pomonella (59, 126), and in comp/eta , first flies may emerge as much as five weeks before walnut husks are susceptible to oviposition (36, 133). Therefore, the time at which a given variety of fruit becomes susceptible to oviposition must be considered as an addi­ tional important criterion for proper timing of the firstprotective insecticide applica­ tion. In cerasi, emphasis for proper timing has shiftedrecently in Switzerland from first fly appearance to reduction of insecticide residues at harvest. This became possible

with the almost exclusive use of systemic insecticides for cerasi control (33). Meth­ ods for precisely predicting cherry harvest have been introduced as an additional element in the existing forecasting system (167). Once the fruit becomes susceptible to oviposition, techniques are required for assessing fly abundance on the host and for accurately relating fly densities to fruit infestation levels. Traps are receiving increasing use for sampling fly populations. The most effective Rhagoletis traps, which capture both sexes, are visual or combi­ by U.S. Department of Agriculture on 12/09/10. For personal use only. nation visual-odor types coated with a sticky substance. The visual aspect consists of (a ) a yellow-colored surface (67), usually a daylight fluorescent yellow rectangle Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org (114, 157), which is believed to constitute a supernormal foliage-type stimulus that elicits food-seeking and/or host-plant-seeking behavior of the flies (151); (b) a dark-colored sphere the size of host fruit or larger (136,147, 149), which is believed to constitute a fruit-type stimulus that elicits fly-matingbehavior and/or oviposition

site- seeking behavior (147); or (c) combinations of these two types (40, 96, 172). The odor consists of volatile components of ammonia-type and/or protein hydroly­ sate-type compounds (14, 16, 67, 84, 165, 181, 198) that are believed to elicit fly food-seeking behavior (198). With the possible exception of completa (16), Rhagole­ tis flies appear unresponsive to those synthetic odors (67, 80) that have shown extremely high attractiveness to males of some Dacus and Ceratitis species (17). In fact, Rhagoletis flies sometimes are little responsive to eVen the best feeding-type lures (80). In pomonella , this is especially so as the season progresses (116), possibly because of an age-dependent decrease in feeding by flies (181) and/or a greater 234 BOLLER & PROKOPY

abundance of competing natural food odors. The degree of fly responsiveness to visual aspects of some traps also may change with time and fly maturity (96, 147, 149, 181) and must be taken into account in population estimates based on trapping. The few attempts made to relate trap captures to fruit infestation level (67, 84, 167) have not yet given entire satisfaction, mainly because of the unpredictability of weather during the oviposition period, crop size, and the possibility that current traps may not be sensitive enough to monitor fly populations at the lowest level that causes economic injury.

Chemical Control Application of insecticides will probably remain the backbone of most Rhagoletis management programs until alternative methods that effect an equally high degree of protection against fruit injury can be realistically employed.

COVER SPRAYS WITH CONVENTIONAL INSECTICIDES The history of insecti­ cide application against Rhagoletis has been reviewed (19, 143, 185) and can be summarized as follows: at first, application was aimed at elimination of adults prior to oviposition through use of arsenicals (87, 98, 185) or DDT (57, 197), and only with the introduction of organophosphates and carbamates, especially systemics, has emphasis of control shifted in some species from the adult to the egg and larval stages. Lead arsenate, both a toxicant and chemosterilant, is still in use against pomonella in the Canadian Maritime Provinces and has shown only moderately adverse effects on beneficialpredators (105, 129). However, both lead and arsenic are unacceptably dangerous environmental pollutants. Systemic organophosphates, such as dimetho­ ate, are highly effective to a wide range of Rhagoletis species (5, 12, 33, 133); act as ovicides, larvicides, and adulticides; and are at present probably the most accept­ able materials for cover sprays against Rhagoletis, although their detrimental side effects to a variety of beneficial insects have been indicated (132). Use of ultra low volume sprays has been reported (85, 2(0)and will be followed with interest. There are apparently no known instances of any Rhagoletis having developed resistance by U.S. Department of Agriculture on 12/09/10. For personal use only. to insecticides, except for the slight resistance of a Connecticut pomonella popula­ tion to DDT (99), which has been banned from agricultural use in most countries. Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org

SELECTIVE CONTROL PROCEDURES Recent research has aimed at achieving selectivity by (a ) limiting treatments to only certain parts of the plant, mainly by bait sprays (40, 62, 78, 126); (b) destruction of pupae and ec10sing adults by application of insecticide to the soil under host plants (107, 135, 185, 193); and (c) development and application of selectively acting chemicals, especially those that interfere with insect development. Studies on the latter are conducted by Vallo and associates on cerasi (190) and by Pree on pomonella (144), both working with juvenile hormone (JH) analogs. Pree explored the possibility of applying the analogs to the soil and could achieve an almost complete elimination of emerging pomonella adults (144). This approach might well occupy a role in regional integrated control programs if more reliable' and safer materials could be found and the problem of immigrating flies alleviated. BIONOMICS AND MANAGEMENT OF RHAGOLETIS 235

An interesting experiment was reported by DePietri-Tonelli and associates (60), who painted small portions of cherry tree trunks with a systemic organophosphate and obtained a high level of larval mortality of cerasi in the fruit. Surprisingly, there has been no followup on this approach, especially in view of its potential for less harm to beneficial insects. Nor has there been investigation of the feasibility of injecting systemic pesticides into the trunk, an approach that would promise an even higher degree of ecological selectivity (134).

Cultural Practices

Removal or destruction of infested fruit was the principal method of Rhagoletis control until the advent of the arsenicals (19, 82, 185). Many early workers felt that cultivating or disking the soil under host trees might reduce Rhagoletis populations, but this proved not to be the case (36, 47, 138, 185). On the other hand, the periodic burning of blueberry plantations and the mowing or removal of nonhost plants prevented buildup of mendax populations (98). A principle threat to the success of current and developing Rhagoletis management techniques is the presence of wild or abandoned hosts near commercial plantings. Removing them, although desirable for Rhagoletis control, might not be feasible for various reasons, and their Rhagole­ tis popUlations will require special attention. Early picking of cherries (23, 102, 185) and a shift to earlier cherry varieties in Europe are important factors contributing to the reduction of cerasi populations.

Biological Control

Although natural enemies have been studied and reviewed in most economically important Rhagoletis species (see section on biology of populations), their effect has proven insufficient for suppression of Rhagoletis populations below economic thresholds. There is no known case where parasites or predators were used success­ fully in management. Clausen's introduction of parasites into California against

completa, indijferens, and Jausta (53) is the only documented record of parasite releases, but the results were negative. Parasites and predators, however, can play

by U.S. Department of Agriculture on 12/09/10. For personal use only. an important role in reducing Rhagoletis populations on wild and abandoned trees close to orchards (117, 118) and will be valuable components of a more complex Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org integrated control strategy. Vallo's success in rearing Phygadeuon wiesmanni, the potent pupal parasite of cerasi, on Ceratitis capitata as alternate host is a significant step forward toward a future parasite management (V. Vallo, personal communica­ tion). Parasites might be exploited for controlling Rhagoletis species that attack processing fruits (i.e. for cider, jam, or distillation), which can tolerate moderate infestation levels.

Attractants and Repellents

Both attractants and repellents have the potential to play a significant role as techniques of direct control in Rhago/efis management programs. In fact, success has already been achieved in reducing high populations of cerasi and pomonella to an economically acceptable level solely by using traps (155, 166, 172). In cerasi, traps are used to reduce natural populations prior to release of sterile flies and to 236 BOLLER & PROKOPY

intercept immigrating fliesin bufferzones around commercial orchards where sterile insect release programs are being conducted (166). Development and incorporation of olfactory lures more powerful and persistent than the existing feeding-type lures into visual traps could produce highly attractive trapping systems, which could be used as alternative control methods in future programs. Whether the so-far unidentified male sex pheromone in pomone/la and the attractive host fruit odors are of this sort remain to be seen. With regard to repellents, if the ovioposition-deterring fruit-marking pheromones of some Rhagoletis could be identified, synthesized, and incorporated into a spray, such materials might reduce or inhibit egg laying, especially if designated plants within or near the orchard were equipped with traps to attract and capture the deterred females (154).

Sterile Insect Technique Although experimental small-scale releases of sterile pomonella flies achieved some reduction of fecundity and fertility in a small field population (139), there is general agreement among Rhagoletis workers that lack of isolation of commercial orchards and abundance of neglected trees are the main obstacles for a potential use of the sterile insect technique (SIT) against Rhagoletis in most of North America. This is especially the case in the eastern part of the continent, although such an approach might be considered for comp/eta in the west and possibly also for in differens in the northwest, where isolated areas are abundant. In Europe, cerasi has been considered a prime candidate for SIT programs ever since ecological studies showed that natural mortality factors alone were not suffi­ cient to reduce populations below the economic threshold (23, 30, 103).

STERILIZATION STUDIES Glogowski (75) was the first to report sterilization of . cera si pupae by irradiation. However, Adam (2) demonstrated induction of somatic damages by pupal irradiation. These disadvantages were alleviated by gamma ir­ radiation of adults (32). The firstreport of a chemosterilant in Rhagoletis deals with lead arsenate showing sterilizing effects on pomone/la (141). Since then, many by U.S. Department of Agriculture on 12/09/10. For personal use only. compounds were tested in pomone/la (139) and ce ra si (2, 190). Adam (2) is the only

Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org author who reports a field experiment that combines visual traps and chemosteri­ lants. The partial failure of this experiment may have been caused by the inadequate choice of the attractant. As mature Rhagoletis spend so much time on the fruit, the realization of field chemosterilization as a practical control method will depend on the development of chemosterilants without effects on mammals.

SIT FIELD PROGRAMS The objectives of a joint SIT research program in Europe for control of cerasi in isolated areas were reported by the four participating labora­ tories in Austria, Czechoslovakia, Germany, and Switzerland (29). Unlike other SIT programs aimed at suppression of the target species, ce ra si programs in progress aim at complete elimination of the pest after three years of releasing sterile flies, followed by a maximum period during which no insecticides must be applied to ripening fruits. First releases were carried out in 1972 in Switzerland with 150,000sterile flies BIONOMICS AND MANAGEMENT OF RHAGOLETIS 237

in order to test logistic and technological problems (31) . In 1973, control experi­ ments were conducted in Switzerland and Austria, and in 1974 in Switzerland, Austria, and eastern Czechoslovakia (27). The data available from these fieldexperi­ ments, which were carried out in relatively small cherry orchards and partly with high densities of wild populations, suggest that the SIT is a promising approach that should be pursued further. There is general agreement among the specialists con­ cerned that the SIT program on cerasi has reached the end of its research phase. Larger experiments involving up to 1400cherry trees are considered the next logical step in the developmental phase and are either in preparation or progress. The SIT is applicable in special situationsJ but has not been considered a general alternative for a broad and generaIly applicable integrated control program.

Genetic Control Ever since the discovery of geneticaIly incompatible populations in cerasi (28) , the potential use of this phenomenon has been discussed. However, present knowledge of the spatial distribution of this interesting trait and the mechanisms involved does not permit a realistic projection of applicability (27).

Host Plant Resistance As mentioned earlier, some fruits receiving Rhagoletis eggs support no larval devel­ opment, and others very little (36, 72, 123, 185). The potential thus exists for breeding varieties tolerant or resistant to Rhagoletis injury. How much such a characteristic might count as compared to all other traits under selection for com­ mercial propagation is uncertain.

CONCLUSIONS

New insight was gained by the authors during the preparation of this review with respect to significant changes in Rhagoletis research over the period of some 100 years covered by the literature. Whereas previously research was carried out by individuals, especiaIly in Europe, a movement toward international cooperation and

by U.S. Department of Agriculture on 12/09/10. For personal use only. pooling of knowledge and resources can now be observed. This trend, stimulated above all by mutual activities of fruit fly workers in the framework of the Interna­

Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org tional Biological Programme, is especially pronounced in Rhagoletis research in­ volving cerasi in Europe and pomonella in North America. A working group of the International Organization for Biological Control (IOBC) on cerasi was established in 1970, with fruit fly specialists of Austria, Germany, Czechoslovakia, and Switzer­ land as full members. This international collaboration and coordination of research efforts has proven valuable in investigating complex problems such as host-race formation and development of SIT programs, which would have been beyond the capacity of individuals. A similar regional working group of Rhagoletis workers was established in 1974 in eastern North America (W.T.A. Neilson, personal communi­ cation). Research on Rhagoletis, both in Europe and North America, has greatly inten­ sified during the last decade, tackled new problems, and utilized new technologies. 238 BOLLER & PROKOPY

Indeed, several Rhagoletis characteristics, such as symbiotic relations with microor­ ganisms, the comparative ease with which individuals in nature can be observed, the relatively short distances over which movement occurs, the tendency to establish insular-type populations on introduced hosts, and the amenability to laboratory handling render Rhagoletis a highly rewarding group in which to study an array of biological concepts and new approaches to insect management. In spite of recent progress, we still have only marginal understanding of such basic processes as food, mate, and host selection in Rhagoletis and only partial knowledge of the principal agents of their mortality. Some phenomena of Rhagoletis biology remain a mystery. For example, pomonella has been recorded numerous times infesting fruits such as pears, cherries, and plums. These infestations sometimes continued for several years but then died out. Explanations for this decline, and for the fact that pomonella has not become established in western North America or Europe, pose a stimulating challenge to Rhagoletis workers. We have pointed out the low tolerance of Rhagoletis injury in commercial fruit. Because integrated methods of Rhagoletis control are still in development-none having been established on a commercial level-insecticides will probably remain the main tool for controlling the economically important Rhagoletis in many re­ gions. Yet, for no Rhagoletis do we know the precise circumstances under which insecticide application is required to prevent economic injury. Visual or visual-odor fly traps are receiving increased attention in monitoring and control of Rhagoletis populations, but so far no one has been able to predict the level of fruit infestation based on the fly catch weeks before harvest. With current traps it might be difficult to establish this relationship, especially when the fly population is low but enough to cause economic injury. New approaches to the improvement of traps are needed, especially with respect to finding more powerful olfactory lures. Wright's theories of olfaction and their recent application in Dacus oleae (182) might have interesting potentials in this respect. Electrophysiological techniques are now being used to investigate Rhagoletis vision (M. Huettel and associates, personal communication), but no one has yet applied them to investigating olfactory re­ sponses in Rhagoletis. by U.S. Department of Agriculture on 12/09/10. For personal use only. We have pointed out that predation on pupating larvae and pupae of Rhagoletis may sometimes reach high levels, but we have only marginal knowledge of the Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org specificorganisms responsible. No one has investigated the influence of the composi­ tion of the understory or neighboring vegetation on the degree of Rhagoletis preda­ tion. Nor have attempts been made so far to mass-produce indigenous parasites and release them against Rhagoletis as a self-perpetuating mortality factor in extensively managed plantations. , Techniques of Rhagoietis management must be coordinated with practices of managing other pests that attack the same crop, as well as with horticultural practices in general. However, it might become necessary to implement integrated control procedures on a regional basis to increase efficacy of action and expertise of responsible personnel. Only with greater attention to the entire crop ecosystem, instead of just to a small portion of it, will we realize the full promise of integrated pest control. BIONOMICS AND MANAGEMENT OF RHAGOLETIS 239

ACKNOWLEDGMENTS

We extend our thanks to those who provided reprints and copies of manuscripts, especially to V. Vallo, who provided access to the eastern European literature by his bibliography and translations. We are grateful to the librarians at Madison, Wisconsin; Sturgeon Bay, Wisconsin and Wiidenswil for their generous support and to Mrs. M. Flury for help in preparing the manuscript.

Literature Cited I. Aczel, M. L. 1954. Gcncros y cspccics nition and bionomics. III. BioI. Monogr. de la tribes "Trypetini." 3. Sobre los No. 26: 194 pp. generos Rhagoletis, Phorellia y To mo­ 12. Bancroft, R. P., Pree, D. J., Toews, plagiodes. Dusenia 5:71-95 D. P. 1974. Comparative toxicities of 2. Adam, H. 1971. Ergebnisse tiber ver­ some insecticides to the apple maggot. gleichende Untersuchungen bei der An­ J. £Con. En tomol. 67:481-83 wen dung von Rontgenstrahlen und 13. Banham, F. L. 1971. Native hosts of Chemosterilantien auf das Reproduk­ western cherry fruit flyin the Okanagan tionssystem von Rhagoletis cerasi L. valley of British Columbia. J. Entomol. Acta Phytopathol. Acad. Sci. Hung. Soc. Br. Columbia 68:29-32 6:281-85 14. Banham, F. L. 1973. An evaluation of 3. Ahmad, M., Carl, K. 1965. The natural traps for the western cherry fruit fly. J. 70: 13-16 enemies of Rhagoletis in Europe. DeM­ En tomol. Soc. Br. Co lumbia 15. 1959. mont Comm. Inst. BioI. Co ntr. Rep. Barnes, M. M. Radiotracer label­ 9 pp. ing of a natural tephritid population 4. AliNiazee, M. T. 1974. The western and flight range of the walnut husk fly. 52:90-92 cherry fruit fly, Rhagoletis indifferens. Ann. Entomol. Soc. Am. 16. Barnes, M. M., Osborn, H. T. 1958. At­ 2. Aggressive behavior. Ca n. Entomol. 106: 1021-24 tractants fo r the walnut husk fly. J. 51 :686-98 5. AliNiazee, M. T. 1974. Chemicals for £Con. Entomol. 17. Bateman, M. A. 1972. The ecology of control of the western cherry fruit fly. 17:493- 65:109-10 fruit flies. Ann. Rev. Entomol. Proc. Oreg. HorNc. Soc. 518 6. AliNiazee, M. T., Brown, R. 0. 1974. A 18. Beck, D. E. 1932. Life-history notes and bibliography of north American cherry a study of the effects of humidity on fruit flies. Bull. Entomol. Soc. Am. c 2:93-101 adult emergen e of Rhagoletis mavis Cress. from pupae at a constant temper­ 7. 1933. Allen, T. C., Fluke, C. L. Notes ature. 1.NY Entomol. Soc. 40:497-99 on the life-history of the apple maggot 19. Beyer, A. H., Hanna, M. 1970. An ac­ in Wisconsin. J. Econ. Entomol. 26: count of early regulatory efforts to con­ 1108- 12 by U.S. Department of Agriculture on 12/09/10. For personal use only. trol cherry fruit fliesin Michigan. Mich. 8. Allen, T. C., Pinckard, J. A., Riker, En tomol. 3:90-96 A. J. 1934. Frequent association of 20. Biggs, J. D. 1972. Aggressive behavior Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org Phytomonas melophthora with various in the adult apple maggot. Ca n. En­ stages in the life cycle of the apple mag­ tomol. 104:349-53 got, Rhagoletis pomonella. Phytopa­ 21. Boller, E. 1964. Auftreten der Kir­ thology 24:228-38 schenfliege (Rhagoletis cerasi L.) und 9. Baerwald, R. J., Boush, G. M. 1967. Prognose mittels Bodentemperaturen Selection of a non-diapausing race of im Jahre 1963. Schweiz. Z. Obst We in­ apple maggot. J. Econ. Entomol. 60: bau 73:53-58 682-84 22. Boller, E. 1965. Beitrag zur Kenntnis 10. Baerwald, R. J., Boush, G. M. 1968. der Eiablage und Fertilitat der Kir­ Demonstration of the bacterial symbi­ schenfliege, Rhagoletis cerasi L. Mitt. ote Pseudomonas melophthora in the Schweiz. Entomol. Ges. 38: 193-202 apple maggot, Rhagoletis pomonella, by 23. Boller, E. 1966. Der Einfluss natiir­ fluorescent-antibody technique. 1. In­ licher Reduktionsfaktoren auf die Kir­ vertebr. Pa thol. 11:25 1-59 schenfliege, Rhagoletis cerasi L. in der 11. Balduf, W. V. 1959. Obligatory and fac­ Nordwestschweiz, unter besonderer Be­ ultative insects in rose-hips, their recog- riicksichtigung des Puppenstadiums. 240 BOLLER & PROKOPY

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210 the apple maggot. J. Econ. Entomol. . 24. Boller, E. 1968. An artificialovipositi on 60:91 8-20 device fo r the European cherry fruit fly, 36. Boyce, A. M. 1934. Bionomics of the Rhagoletis cerasi L. J. £Con. Entomol. walnut hush fly, Rhagoietis comp/eta. 61:850-52 Hilgardia 8:363-579 25. BoUer, E. F. 1972. Behavioral aspects of 37. Brittain, W. H., Good, C. A. 1917. The mass-rearing of insects. Entomophoga apple maggot in Nova Scotia. Bull. NS 17:9-25 Dep. Agric. 9:1-70 26. Boller, E. F. 1976. Life table studies and 38. Brooks, F. E. 1921. Walnut husk mag­ pupal mortality in fruit flies. IBP Syn­ got. US Pep. Agric. Bull 992:1-8 thesis Rep. , Cambridge, Eng!.: Cam­ 39. Buriff, C. R. 1973. Recapture of re­ bridge Univ. Press In press leased adult apple maggot flies in sticky­ 27. Boller, E. F. 1974. Progress Report of board traps. Environ. EntomoL 2: the IOBC Wo rking Group on Genetic 757-58 Control of Rhagoletis cerasi L. Pre­ 40. Buriff, C. R., Still, G. W. 1973. Black sented at General Assembly of cherry fruit fly: bait spray for control. IOBC/WPRS, Madrid, 1974 J. £Con. Entomol 66: 1350-5 1 28. Boller, E. F., Bush, G. L. 1974. Evi­ 41. Bush, G. L. 1966. The taxonomy, dence for genetic variation in popula­ cytology and evolution of the genus tions of the European cherry fruit fly, Rhagoletis in North America. Bull. Rhagoletis cerasi L. based on physiolog­ Mus. Compo Zool Harv. Un iv. 134:431- ical parameters and hybridization stud­ 562 ies. Entomol. Exp. Appl. 17:279-93 42. Bush, G. L. 1969. Sympatric host race 29. Boller, E. F., Haisch, A., Russ, K., formation and speciation in frugivorous Vallo, V. 1970. Economic importance flies of the genus Rhagoletis. Evo/ution of Rhagoletis cerasi L., the feasibility of 23:237-51 genetic control and resulting research 43. Bush, G. L. 1974. The mechanism of problems. En tomophaga 15:305-13 sympatric host race formation in the 30. Boller, E. F., Haisch, A., Prokopy, R. I. true fruit flies. In Genetic Mechanisms 1971. Sterile insect release method of Sp eciation in Insects, ed. M . J. D. against Rhagoletis cerasi L. Prepara­ . tory ecological and behavioral studies. White, 3-23. Sydney: Australian & New Zealand Book Co. Sy mp. Sterility Princip le fo r Insect Con­ 44. Bush, G. L. 1975. Sympatric speciation trol or Eradication. IA EA Athens, 1970 77-86 in phytophagous parasitic insects. In , Evolutionary Strategies f Parasitic In­ 31. Boller, E. F., Remund, U. 1974. The o application of the sterile insect release sects, ed. P. W. Price. New York: Ple­ method against the European cherry num. In press fruit fly, Rhagoletis cerasi L. in north­ 45. Bush, G. L., Huettel, M. D. 1976. Pop­ west Switzerland. IAEA Proc. Ser. The ulation and ecological genetics of fruit Sterile-Insect Te chnique and Its Fie/d flies. In IBP Sy nthesis Rep. Cambridge, Cambridge Press by U.S. Department of Agriculture on 12/09/10. For personal use only. Applications, 1-3 Eng\.: Univ. In press 32. Boller, E. F., Remund, U., Zehnder, J. 46. Caesar, L., Ross, W. A. 1919. The apple 1975. Sterilization and quality control maggot. Bull. Onto Dep. Agric. 271:1-32 Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org of the European cherry fruit fly, Rha­ 47. Caesar, L., Spencer, G. J. 1915. Cherry go/etis cerasi L. Sy mp. Sterility Principle fruit flies. BulL Onto Dep. Agric. 227: fo r Insect Control, IA EA 1974, (In nsb­ 30 pp. ruck), 179-89 48. Cameron, P. I., Morrison, F. O. 1974. 33. Boller, E., Wildbolz, T. 1965. Neue Sampling methods for estimating the Wirkstoffe flir die Kirschenfliegen­ abundance and distribution of all life bekampfung. Sch weiz. Z Obst We inbau stages of the apple maggot, Rhagoletis 74:7-8 pomonella. Ca n. Entomol, 106:1025-34 34. Boush, G. M., Baerwald, R. J., 49, Carl, K. P. 1968. Collection of and ob­ Miyazaki, S. 1969. Development of a servation on the natural enemies of chemically defined diet for adults of the Rhago/etis cerasi L. Pe!emont Comm. apple maggot based on amino-acid anal­ Inst. BioI. Contr. Rep. 8 pp. ysis of honey-dew. Ann. Entomol. Soc. 50. Chapman, P. J., Hess, A. D: 1941: Mor­ Am. 62:19-2 1 tality of the apple maggot In frUIt held 35. Boush, G. M., Matsumara, F. 1967. In­ in cold storage. Cir. US Pep. Agric. secticidal degradation by Pseudomonas 600:1-9 BIONOMICS AND MANAGEMENT OF RHAGOLETIS 24 1

51. Christenson, L. D., Foote, R. H. 1960. fruit fliesin EasternWashington. Wash. Biology of fruit flies. Ann. Rev. En­ Agrie. Exp. Sta. Te ch. Bull. 13:66 pp. tomol. 5:171-92 68. Frings, H., Frings, M. 1955. The loca­ 52. Cirio, U. 1972. Osservazioni sui com­ tion of the contact chemoreceptors of portamento di ovideposizione della the cherry fruit fly. Rhagoletis cin­ Rhagoletis completa Cress. in laborato­ gulala, and the fleshfly, Sarcophaga buf­ rio. Proc. Congr. Ital. Entomol., 9th, Iota. Am. MidI. Not. 53:431-35 Siena 99-1 17 69. Fytizas, E. 1973. Influence d'une seule 53. Clausen, C. P. 1956. Biological control administration de levure hydrolysee sur of fruit flies. J. Econ. Entomol. 49: la fecondite des fe melles de Dacus oleae 176-78 Gmel. Ann. Zoo!. Beol. Anim. 5:39-44 54. Dean, R. W. 1935. The anatomy and 70. Garman, P. 1936. Studies in breeding postpupal development of the female re­ and control of the apple maggot. Conn. productive system in the apple maggot Agric. Exp. Sta. Bull 383:315-20 fly, RhagoJetis pomoneJ/a Walsh. Tech. 71. Girolami, V. 1973. RepeTti morfo­ Bull. NY State Agrie. Exp. Sta. istologici sulle batteriosimbiosi del 229:1-31 Dacus oleae Gmel. e di altri ditteri 55. Dean, R. W. 1938. Experiments on tripetidi, in natura e negli allevamenti rearing apple maggot adults. J £Con. su substrati artificiali. Redia 54:269-94 Entomol. 31 :241-42 72. Glasgow, H. 1933. The host relations of 56. Dean, R. W. 1942. Emergence, migra­ our cherry fruit flies. J. Eeon. Eneomof. tion and control of the apple maggot fly. 26:431-38 Proe. NY State Hortie. Soc. 87:291-95 73. Glass, E. H. 1960. Apple maggot fly 57. Dean, R. W. 1947. Apple maggot con­ emergence in western New York. Bull. trol with DDT sprays and dusts. J. NY State Agric. Exp. Sta. 789:1-29 Econ. Entomol. 40:183-89 74. Glass, E. H., Chapman, P. J., Smock, 58. Dean, R. W. 1969. Infestation of R. M. 196 \. Fate of apple maggot and peaches by Rhagoletis suavis. J Eeon. plum curculio larvae in apple fruits held Entomol. 62:940-41 in controlled atmosphere storage. J. 59. Dean, R. W., Chapman, P. J. 1973. Bio­ Beon. Entomol. 54:915-18 nomics of the apple maggot in Eastern 75. Glogowski, K. 1967. Wplyv roznych New York. Search Agrie. Entomol. davek promieny roentgena na smiertel­ Geneva 3:62 pp. nose i rozmnazanie nasionnicy trzesni­ 60. De Pietri-Tonelli, P., Barontini, A., owiki, Rhagoletis cerasi L. Pro Na uk. Biondi, G. 1962. Systemic migration and insecticidal activity of dimethoate [nst. Oehr. Rosi. 9':263-70 76. Haefliger, E. 1953. Das Auswahlvermo­ applied on tree trunks. Proc. Br. Insect. gen der Kirschenfliegebei der Eiablage. Fu ngie. Con/. 1961 Sussex 2:407-32 61. Doane, R. W. 1898. A new trypetid of Mitt. Sch weiz. Entomol. Ges. 26:258-64 economic importance. Entomol. News 77. Hagen. K. S. 1958. Honeydew as an 9:69-72 adult fruit fly diet affecting reproduc­ 62. Dolphin, R. E., Cleveland, M. L., Still, tion. Proe. 10th Int. Congr. Entomol., by U.S. Department of Agriculture on 12/09/10. For personal use only. G. W., Mouzin, T. E. 1970. Reduction Montreal 1956 3:25-30 of populations of apple maggots with 78. Hagen, K. S., Tassan, R. L. 1972. Ex­ ploring nutritional roles of extracellular

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81. Hall, J. A. 1939. Further observations emergence of Rhagoletis pomonella. J. on the biology of the apple maggot Econ. En (omol. 38:330--34 (Rhagoletis pomonella Walsh). Ann. 98. Lathrop, F. H., Nickels, C. B. 1932. Rep. Enlomol. Soc. ant. 69:53-58 The biology and control of the blue­ 82. Harvey, F. L. 1890. The apple maggot. berry maggot in Washington County, Rep. Maine Agric. Exp. Sta. 1889: 190-- Me. US Dep. Agric. Te ch. Bull. 275: 24 1 76 pp. 83. HeIlmuth, H. 1956. Untersuchungen 99. Leonard, D. E. 1961. Development of zur Bakteriensymbiose der Trypetiden. resistance to DDT by the apple maggot, Z. Morphol. Oekol. Tiere 44:483-5 17 Rhagoletis pomonella. 1. Econ. En­ 84. Hodson, A. C. 1948. Further Studies of tomol. 54:880-82 lures attractive to the apple maggot. J. 100. LeRoux, E. J., Mukerji, M. K. 1963. Econ. Entomol. 41 :61-66 Notes on the distribution of immature 85. Howitt, A. J., Nelson, J. W., Roberts, stages of the apple maggot, Rhagoletis 1964. W. W. A comparison of low vol­ pomonella (Walsh) on apple in Quebec. ume aerial spraying and dusting in the Ann. Entomol. Soc. Quebec 8:6{}-70 control of blueberry maggot, Rhagoletis 101. LeRoux, E. J., Reimer, C. 1959. Varia­ pomonella (Walsh). Bull. Mich. State tion between samples of immature Un iv. Agric. Exp. Sta. 47:246--58 stages, and of mortalities from some 86. Hoyt, S. c., Burts, E. C. 1974. Inte­ factors, of the eye-spotted budmoth grated control of fruit pests. Ann. Rev. Sp ilonota ocellana D.&S., and the pistol 19:23 1-52 Entomol. casebearer, Coleophora serratella L. on 87. 1912. Illingsworth, I. F. A study of the apple .in Quebec. Ca n. Entomol. 91: apple maggot (Rhagoletis pomonella ) 428-49 together with an investigation of meth­ 102. Leski, R. 1963. Studies on the biology ods of control. Bull. NY State Agric. and ecology of the cherry fruit fly, Rha­ Exp. Sta. 324: 1 25-88 88. 1912. goletis 'cerasi L. Pol. PLfmo Entomol. Illingsworth, I. F. Cherry fruit 3 1/32: 1 54-240 flies and how to control them. Bull. NY 103. Leski, R. 1969. Population studies of State Agric. Exp. Sta. 325:191-204 the cherry fruit fly, Rhagoletis cerasi L. 89. Jermy, T. 1961. Eine neue Rhagoletis­ Proc. IAEA/FA O Pa nel Insect Ecology Art aus den Friichten von Berberis vul­ and the Sterile-Male Te chnique, Vie nna garis L. Acta Zool. A cad. Sci. Hung. 1-7 7:133-37 1967. 104. Lindgren, D. L. 1955. Effect of 90. Jones, S. C., Wallace, L. 1955. Cherry acrylonitrile fumigation on diapause in fruit flydispersion studies. J. Econ. En­ 48:616-17 the walnut husk fly. J. Econ. Entomol. tarnal. 48:752-53 91. Jubb, G. L., Cox, J. A. 1974. Seasonal 105. MacPhee, A. W., MacLellan, C. R. emergence of two cherry fruit flyspecies 1971. in Erie County, Pennsylvania: 25-year Ecology of apple orchard fauna and development of integrated pest con­ summary. J. Econ. Entomol. 67:613-15 92. Kalandadze, L. P., Bagdavadze, A. I. trol in Nova Scotia. Proc. Ta ll Timbers by U.S. Department of Agriculture on 12/09/10. For personal use only. 1956. Biologiceskie osobennosti vis­ Conf Ecol. Anim. Co ntr. Ha bitat Ma n­ 3: 197-208 nevoj muchi, Rhagoletis cerasi L., v age. 1177-85 106. Marcovitch, S. 1915. The biology of the Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org Gruzinskoj SSR. Zool. Zh. 35: 93. Kamal, A. S. 1954. Ecological and nu­ juniperberry insects, with descriptions tritional studies on the cherry fruit fly. of new species. Ann. Entomol. Soc. Am. 8:163-79 J. Econ. Entomol. 47:959-65 94. Klein-Krautheim, F. 1937. Ueber die 107. Maxwell, C. W., .Parsons, E. C. 1962. Hagenbuttenfliege (Rhagoletis alternata Comparison of soil surface treatment of Fall.). Z. Angew. Entomo!. 23:603-14 some fumigants and soil insecticides fo r 95. Knell, J., Stoffolano, J. G. 1973. His­ apple maggot control. 1. Econ. En­ tology of the third instar of the apple tarnal. 55: 1022-23 maggot, Rhagoletis pomonella. Ann. 108. Maxwell, C. W., Parsons, E. C. 1968. Entomol. Soc. Am. 66:1221-38 The recapture of marked apple maggot 96. Kring, J. B. 1970. Red spheres and yel­ adults in several orchards from one re­ low panels combined to attract apple lease point. J. Econ. Entomol. 61: maggot flies. J. Econ. Entomol. 63: 1157-59 466-69 109. Maxwell, C. W., Parsons, E. C. 1969. 97. Lathrop, F. H., Dirks, C. 0. 1945. Tim­ Relationships between hour-degree F ing the seasonal cycles of insects: the soil temperature summations and apple BIONOMICS AND MANAGEMENT OF RHAGOLETIS 243

maggot adult emergence. J. Econ. En­ goletis pomonella, in crab apples. Ca n. tomol. 62:1310-13 Entomol. 99:217-19 110. McAlister, L. C. 1932. An observation 124. Neilson, W. T. A. 1971. Dispersal stud­ of a maggot, Rhagoletis pomonella ies of a natural population ofapple mag­ Walsh, passing from one blueberry into got adults. J. Econ. Entomol. 64;648-53 an adjacent blueberry. J. Econ. En­ 125. Neilson, W. T. A. 1973. Improved tomol. 25:412-\3 method for rearing apple maggot larvae 111. Middlekauff, W. W. 1941. Some biolog­ from artificial media. J. £Con. Entomol. ical observations of the adults of the ap­ 66;555-56 ple maggot and the cherry fruit flies. J. 126. Neilson, W. T. A., Maxwell, C. W. £Con. Entomo!' 34:621-24 1964. Field tests with a malathion bait 112. Mitic-Muzina, N. 1960. The results of spray fo r control of the apple maggot, studies on the bionomics of the cherry Rhagoletis pomonella. J. Econ. En­ fruit fly near Belgrade. Plant Prot. Bel­ tomol. 57:192-94 grade 60:29-53 127. Neilson, W. T. A., McAllen, J. W. 113. Miyazaki, S., Boush, G. M., Baerwald, 1965. Effects of mating on fecundity of R. I. 1968. Amino acid synthesis by the apple maggot, Rhagoletis pomonella Pseudomonas melop hthora, bacterial (Walsh). Can. Entomol. 97:276-79 symbiote of Rhagoletis pomonella. J. 128. Neilson, W. T. A., McAllen, J. W. Insect Physiol. 14:513-18 1965. Artificial diets for the apple mag­ 114. Moericke, V. 1976. Responses of tephri­ got. III. Improved, defined diets. J. tid flies to color stimuli. IBP Sy nthesis £Con. Entomol. 58;542-43 Rep. , Cambridge, Eng!.: Cambridge 129. Neilson, W. T. A., Patterson, N. A., Univ. Press In Press Pickett, A. D. 1968. Field and labora­ 115. Moericke, V., Prokopy, R. J., Ber­ tory studies with lead arsenate for con­ locher, S., Bush, G. L. 1975. Visual trol of the apple maggot in Nova Scotia. stimuli associated with attraction of J. Econ. Entomol. 61;802-805 Rhagoletis pomonella flies to trees. En­ 130. Neilson, W. T. A., Sanford, K. H. 1974. tomol. Exp. Appl. In press Apple maggot control with baited and 116. Moore, R. C. 1969. Attractiveness of un baited sprays of azinphos-methyl. J. baited and unbaited lures to apple mag­ £Con. Entomol. 67:556-57 got and beneficial flies. J. Econ. En­ 131. Neilson, W. T. A., Wood, F. A. 1966. tomol. 62: 1076-78 Natural source of food of the apple 117. Monteith, L. G. 1971. Crickets as maggot. J. Econ. Entomol. 59:997-98 predators of the apple maggot, Rhagole­ 132. Neilson, W. T. A., Wood, G. W., Max­ tis pomonella. Ca n. Entomol. 103:52-58 well, C. W. 1970. Dimethoate sprays for 118. Monteith, L. G. 1971. The status of apple maggot and their effect on preda­ parasites of the apple maggot, Rhagole­ cious insects and mites. J. Econ. En­ tis pomonella in Ontario. Ca n. Entomol. tomol. 63:764-66 103:507-12 133. Nickel, J. L., Wong, T. T. Y. 1966. Con­ 119. Monteith, L. G. 1972. Status of preda­ trols of the walnut husk fly, Rhagoletis tors of the adult apple maggot, Rhagole­ completa Cresson, with systemic insec­

by U.S. Department of Agriculture on 12/09/10. For personal use only. tis pomonella in Ontario. Ca n. Entomol ticides. J. £Con. Entomol 59;1079-82 104;257-62 134. Norris, D. M. 1967. Systemic insecti­ 120. MUller, W. 1970. Agrarmeteorologi­ cides in trees. Ann. Rev. Entomol. Annu. Rev. Entomol. 1976.21:223-246. Downloaded from www.annualreviews.org sche Untersuchungen Uber das Erstauf­ 12;127-48 treten der Kirschenfliege (Rhagoletis 135. Oatman, E. R. 1964. Residual effective­ cerasi L.) in Oesterreich. Pjl anzen­ ness of endrin as a soil insecticide for schutzberichte 41;192-209 control of the apple maggot in Wiscon­ 121. Neilson, W. T. A. 1962. Effects of tem­ sin. J. Econ. Entomol. 57:163-64 perature on development of overwinter­ 136. Oatman, E. R. 1964. Apple maggot trap ing pupae of the apple maggot, Rhagole­ and attractant studies. J. Econ. En­ tis pomonella (Walsh). Ca n. Entomol. tomol. 57:529-31 94;924-928 137. Oatman, E. R. 1964. Apple maggot 122. Neilson, W. T. A. 1964. Some effects of emergence and seasonal activity in Wis­ relative humidity on development of consin. J. Econ. Entomo!' 57;676-79 pupae of the apple maggot, Rhagoletis 138. O'Kane, W. C. 1914. The apple maggot. pomonella (Walsh). Can. Entomo!' Bull. NH Agric. Exp. Sta. 171:1-120 96:810-11 139. Padula, L. 1970. Comparative effects 0/ 123. Neilson, W. T. A. 1967. Development chemosterilants on the fe cundity, fe r­ and mortality of the apple maggot, Rha- tility, and biology of the app le maggot, 244 BOLLER & PROKOPY

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