Biology, ecology, and management of dogwood borer in eastern apple ...

Color profile: Disabled Composite Default screen

Biology, ecology, and management of dogwood borer in eastern apple orchards 635 J Christopher Bergh1 Department of Entomology, Virginia Polytechnic Institute and State University, Alson H Smith, Jr, Agricultural Research and Extension Center, 595 Laurel Grove Road, Winchester, Virgina 22602, United States of America

Tracy C Leskey USDA–ARS, Appalachian Fruit Research Station, 45 Wiltshire Road, Kearneysville, West Virginia 25430, United States of America The Canadian Entomologist 135: 615 – 635 (2003)

Abstract—The dogwood borer, Synanthedon scitula (Harris) (Lepidoptera: Sesiidae), has the broadest host range of the clearwing moths and is considered to be an economically important pest of many ornamental, fruit, and nut trees. Since the 1980s, dogwood borer has been recognized as an increasingly important, indirect pest of apple, Malus domestica Borkh. (Rosaceae), in eastern North America, owing mainly to increased plantings of apple on size-controlling rootstocks that promote the formation of adventitious root initials (burr knots) on the rootstock and scion. Burr knots appear to be preferred oviposition sites for dogwood borer females, although infestations can also be initiated in wounds, pruning cuts, and crotches on the branches and trunk. Larval feeding in burr knots does not adversely affect the growth and vigor of apple trees, but their mining outward from burr knots into vascular tissue can ultimately cause tree decline and death. Chlorpyrifos is the most effective insecticide for controlling dogwood borer. A supplemental label in the United States permits post-bloom, trunk drench applications of chlorpyrifos specifically for control of borers in apple, with several restrictions that preclude control of infestations higher in the tree. The ongoing review of pesticide tolerances dictated by the 1996 Food Quality Protection Act of the United States of America makes the long-term availability of this chemical uncertain. Cultural practices, such as deeper planting or berming, can reduce the likelihood of infestation of new apple plantings by dogwood borer, although they do not preclude infestations from developing above the graft union. This review and discussion is based on our contention that research toward the development of alternative, behaviorally based management strategies for dogwood borer in apple and other economically important host plants is warranted. Our review and synthesis of the dogwood borer literature revealed important gaps in knowledge about basic aspects of its biology that pertain directly to the development of alternative control tactics based on behavioral manipulation. There is considerable confusion surrounding the sex pheromone of dogwood borer and conflicting results on the response of males to isomers and blends of isomers of its purported pheromone. Studies using sex attractants to monitor its phenology in apple and non-apple habitats have yielded discrepant results and conclusions. Differences in the effectiveness of commercially available pheromone lures for trapping dogwood borer have been reported and the ability of pheromone traps to accurately reflect emergence or population density remains in question. Regardless of pronounced differences in the duration and modality of the seasonal flight of dogwood borer among different geographical regions within its range, the conclusion of univoltinism across most of its range has been perpetuated, based on extremely limited developmental data collected exclusively from individuals that developed on dogwood. 1 Corresponding author (e-mail: [email protected]).

615

J:\ent\ent13505\N02-089.vp August 27, 2003 1:45:27 PM


616

THE CANADIAN ENTOMOLOGIST

September/October 2003

Bergh JC, Leskey TC. 2003. Biologie, écologie et gestion de la sésie du cornouiller dans des pommeraies de l’Est. The Canadian Entomologist 135 : 615–635.

Résumé—La sésie du cornouiller, Synanthedon scitula (Harris) (Lepidoptera : Sesiidae), est le sésiidé qui possède la gamme la plus étendue d’hôtes et elle est considérée comme un ravageur d’importance économique de plusieurs arbres d’ornement, arbres fruitiers et arbres à noix. Depuis les années 1980, la sésie du cornouiller est devenue un ravageur indirect, mais d’importance croissante, du pommier, Malus domesticus Borkh. (Rosaceae), dans l’est de l’Amérique du Nord à cause surtout de la pratique de plus en plus répandue de planter les pommiers sur des porte-greffe qui limitent leur taille et qui favorisent la formation de primordiums de racines adventices (broussins) sur le porte-greffe et sur le greffon. Les broussins semblent être les sites préférés de ponte des sésies du cornouiller, bien que les infestations puissent débuter dans les plaies, les coupures d’émondage et les fourches sur les branches et le tronc. L’alimentation des larves dans les broussins n’affecte de façon négative ni la croissance, ni la vigueur des pommiers, mais le déplacement des larves vers l’extérieur des broussins, dans le tissu vasculaire, peut en fin de compte causer le déclin et la mort de l’arbre. Le chlorpyrifos est l’insecticide le plus efficace pour contrôler la sésie du cornouiller. Une étiquette supplémentaire aux États-Unis d’Amérique permet l’application du chlorpyrifos après la floraison par imprégnation du tronc spécifiquement pour la lutte contre les sésies chez le pommier, mais plusieurs restrictions en défendent l’utilization pour le contrôle d’infestations plus haut dans l’arbre. La mise à jour continuelle des tolérances des pesticides ordonnée par la loi américaine de 1996 sur la protection de la qualité de la nourriture rend la disponibilité de ce produit chimique incertaine à long terme. Des pratiques culturales, telles que de planter les pommiers plus profondément ou d’entasser de la terre le long du tronc, peuvent réduire la probabilité de l’infestation de nouvelles plantations de pommiers par la sésie, bien qu’elles n’empêchent pas les infestations de se développer au-dessus du niveau de la greffe. Notre revue et notre discussion se justifient, croyons-nous, par la nécessité de chercher des stratégies de gestion de rechange, basées sur le comportement, pour faire la lutte à la sésie du cornouiller dans les pommeraies et dans les cultures d’autres plantes d’importance économique. Notre revue et synthèse de la littérature sur la sésie du cornouiller met en lumière d’importantes lacunes dans les connaissances biologiques fondamentales de l’insecte qui sont directement reliées à laconception de stratégies de lutte de rechange basées sur la manipulation des comportements. Il existe beaucoup de confusion au sujet de la phéromone sexuelle de la sésie du cornouiller et des résultats contradictoires sur la réaction des mâles aux isomères ou aux mélanges d’isomères de sa présumée phéromone. Des études qui ont utilizé des substances d’attraction sexuelle pour suivre la phénologie de l’insectes dans des habitats de pommeraies et d’autres milieux ont aussi produit des résultats et des conclusions contradictoires. Les pièges à phéromones disponibles dans le commerce pour capturer la sésie du cornouiller ont des efficacités variables et la capacité de ces pièges de refléter avec précision l’émergence et la densité de population reste à déterminer. Malgré des différences importantes dans la durée et la modalité du vol saisonnier de la sésie du cornouiller dans les différentes régions géographiques de sa répartition, on continue à lui attribuer un cycle univoltin sur presque toute son aire de répartition; ces conclusions se basent sur des données de développement extrêmement succinctes obtenues sur des insectes qui se sont développés sur des cornouillers. [Traduit par la Rédaction]

Introduction The dogwood borer, Synanthedon scitula (Harris) (Lepidoptera: Sesiidae), has been recognized as an economically important pest for nearly 100 years (Herrick 1904)



Volume 135


617

and at least 19 species of fruit, nut, and ornamental trees are recorded hosts (Engelhardt 1932; Eichlin and Duckworth 1988; Johnson and Lyon 1991). As the common name of this insect suggests, the flowering dogwood, Cornus florida L. (Cornaceae), has been considered the most economically important host plant of dogwood borer (Pless and Stanley 1967; Potter and Timmons 1983; Williams et al. 1985) and extensive infestations in dogwood nurseries have been reported (Underhill 1935; Wallace 1945; Rogers and Grant 1990). Eggs are deposited preferentially on or near injured bark (Herrick 1904; Engelhardt 1932; Wallace 1945), through which teneral larva enter the tree and construct feeding galleries. Damage is inflicted when larvae feed on cambial tissue beneath the bark (Underhill 1935; Wallace 1945; Pless and Stanley 1967), rendering trees unmarketable (Rogers and Grant 1990), potentially increasing their susceptibility to disease (Walton 1986), and resulting in partial or complete girdling and the demise of trees (Underhill 1935). Mechanical injury from mowers and other equipment, and exposure to sun, were strongly correlated with infestation of dogwood trees in nurseries and urban landscapes (Potter and Timmons 1981; Rogers and Grant 1990). Pless and Stanley (1967) observed that infested dogwood trees were often susceptible to attack in subsequent seasons, and top-worked pecan trees in Texas were highly susceptible to infestation at pruning cuts (Pierce and Nickels 1941). The low incidence of dogwood borer infestation of native dogwoods in the forest understory has been observed repeatedly (Underhill 1935; Wallace 1945; Pless and Stanley 1967; Rogers and Grant 1990) and attributed to the lack of mechanical injury to trees in those habitats. Owen et al. (1991) found that vinyl tree wraps around the trunk of young dogwood trees significantly increased the incidence of dogwood borer infestation, likely owing to favorable conditions for larval survival. Since the 1980s, dogwood borer has been recognized as an increasingly important pest of apple, Malus domestica Borkh. (Rosaceae), in eastern North America (Riedl et al. 1985; Warner and Hay 1985; Weires 1986; Pfeiffer and Killian 1999; Kain and Straub 2001). Riedl et al. (1985) and Kain and Straub (2001) concluded that the ultimate factor responsible for the increased abundance of dogwood borer in apple is the increasing use of clonal, size-controlling rootstocks in high-density orchards. An identical situation exits in Europe where the congeneric species apple clearwing moth, Synanthedon myopaeformis (Borkh.), infests burr knots on the rootstock of trees planted in high-density orchards (Dickler 1976). Clonal rootstocks promote the formation of adventitious root primordia (burr knots) near the graft union at the base of the tree (Rom 1970, 1973) that appear to be preferred oviposition sites for dogwood borer females (Riedl et al. 1985; Warner and Hay 1985; Kain and Straub 2001). Infestation and larval feeding over consecutive seasons can lead to consumption of burr knot tissue and feeding in the cambial layer, ultimately resulting in tree death from girdling (Weires 1986). Both chemical and cultural options for managing dogwood borer have been demonstrated (Potter and Timmons 1983; Riedl et al. 1985; Warner and Hay 1985; Kain and Straub 2001; Wise and Gut 2002). Of increasing concern, however, is whether the most efficacious, organophosphate pesticides will remain available in the long term, owing to the ongoing review of tolerances by the United States Environmental Protection Agency under the Food Quality Protection Act of 1996. Research on alternative control strategies for dogwood borer, including those based on behavioral manipulation, is limited. Given the commercial applicability of pheromone-based mating disruption of the congeneric species peachtree borer, Synanthedon exitiosa (Say), and lesser peachtree borer, Synanthedon pictipes (Grote and Robinson), this approach appears well suited to dogwood borer. Recently, an attract and kill technology using sex pheromone has been registered for managing codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), in tree fruit and is another potential control option for dogwood borer in



618



apple and ornamental host plants that merits investigation. Successful development of these approaches for dogwood borer, however, will require a more thorough understanding of its life history, chemical ecology, and reproductive behavior than is currently the case. The literature on dogwood borer contains significant inconsistencies in the conclusions drawn from studies of seasonal flight activity using pheromones, conflicting results about the relative attractiveness of commercially available pheromone lures, and important gaps in knowledge about larval developmental rates and their influence on voltinism in apple and other hosts. This paper synthesizes published information on dogwood borer, highlighting those areas where inconsistencies and conflicting or insufficient data influence our understanding of its biology in the apple ecosystem. We suggest lines of research that should resolve outstanding questions concerning dogwood borer biology and ecology in apple and aid in the development of alternative management tactics for this increasingly important pest.

Monitoring adult flight Seasonal phenology Using observational data, Underhill (1935) and Wallace (1945) noted that first flight of dogwood borer in Virginia and Connecticut, respectively, occurred at about the time that flowering shrubs in the genus Weigela (Diervillaceae) began to bloom. Two studies have used degree-day summations and captures in pheromone traps to predict first emergence of dogwood borer. Potter and Timmons (1983) accumulated degree-days from 1 October over 3 consecutive years in urban habitats in Kentucky, using a base temperature of 4°C. Degree-day summations at first capture of males in traps placed in dogwood trees were similar among years and locations, leading Potter and Timmons (1983) to conclude that this method could provide reasonably accurate predictions of first flight. Concurring with earlier reports, Potter and Timmons (1983) also noted that the first capture of males occurred when the genus Weigela began to bloom. Riedl et al. (1985) used the base temperature of 4°C established by Potter and Timmons (1983) to accumulate heat units from 1 October over 3 consecutive years in New York apple orchards. The average degree-day accumulation at the time of first catch of males in pheromone traps was variable, leading Riedl et al. (1985) to conclude that the average date of first catch was a better predictor of emergence. Studies using either observational information or pheromone traps to monitor the seasonal patterns of emergence and flight activity of dogwood borer from several hosts in different ecological settings have yielded results that differ according to geographical location (i.e., latitude) and habitat. The latest onset and shortest duration of flight was recorded from studies in Ontario and Michigan (Table 1). Although reports from New York and Connecticut showed an earlier onset and considerably longer duration of flight than in Michigan and Ontario, data from the four locations indicated a unimodal flight with peaks that coincided closely. From Kentucky and south through Tennessee, dogwood borer showed a bimodal flight pattern, with a trend toward earlier onset of flight in the spring and seasonal flight durations that were generally longer than farther north. Although Snow et al. (1985) suggested that the seasonal flight of dogwood borer in Georgia showed a pronounced, single peak in April and May, their data also revealed the earliest onset and longest duration of flight and could be interpreted as depicting three flight peaks (Table 1). In several studies that recorded bimodal flight patterns (Potter and Timmons 1983; Rogers and Grant 1991; Pfeiffer and Killian 1999; Eliason and Potter 2000), pheromone traps were deployed in different habitats to compare emergence from different hosts. Potter and Timmons (1983) provided evidence that the early flight peak in


Volume 135

J:\ent\ent13505\N02-089.vp August 27, 2003 1:45:30 PM THE CANADIAN ENTOMOLOGIST

NOTE: Periods of peak flight are indicated by the elevated section(s) of each horizontal bar. The studies from each location were reported as follows: Ontario, Warner and Hay (1985); Michigan, Howitt (1993); New York, Riedl et al. (1985); Connecticut, Wallace (1945); Kentucky, Potter and Timmons (1983); Kentucky, Eliason and Potter (2000); Virginia, Pfeiffer and Killian (1999); Tennessee, Rogers and Grant (1991); and Georgia, Snow et al. (1985). * Habitat type: A, apple; U, urban landscape; H, hardwood forest; N, commercial nursery; P, peach; NR, not reported. † From pheromone traps. ‡ From observation data.

TABLE 1. Seasonal flight activity of Synanthedon scitula reported from studies in different habitats and at different latitudes.


619


620



Kentucky consisted primarily of dogwood borer emerging from dogwood, whereas the later peak appeared to have been mainly from apple and possibly other hosts. They suggested that emergence of dogwood borer from apple occurs mainly in August and September. Pfeiffer and Killian (1999) also showed an early peak of trap catch from nonapple hosts in central Virginia, but both early and later peaks from apple. In urban habitats and commercial dogwood nurseries in Tennessee, Rogers and Grant (1991) were unable to relate the later flight peak with emergence from hosts other than dogwood, although they mentioned that few pupal exuviae were found on dogwood trees during the second flight peak. Eliason and Potter’s (2000) study in urban habitats in Kentucky showed similar bimodal emergence of dogwood borer from stands of dogwood and from pin oaks that supported large numbers of dogwood borer infested horned oak galls. Unlike previous studies in Virginia and Kentucky, more moths were trapped during the later flight than during the early flight from both dogwood and galled pin oak sites. Although more pupal exuviae were recovered from dogwood trees during the early flight, the number collected from galls was similar for both flights, leading Eliason and Potter (2000) to conclude that emergence of dogwood borer from horned oak galls did not contribute disproportionately to either flight. Pheromone trap captures compared with other measures of emergence Several studies compared the emergence of dogwood borer with the capture of males in pheromone traps throughout the flight period. To measure emergence, Warner and Hay (1985) collected moths from within screened cages surrounding burr knots on 20 apple trees twice weekly. Riedl et al. (1985) used screened cages around the trunk of 20 apple trees and counts of fresh pupal exuviae on burr knots. Eliason and Potter (2000) examined 23 flowering dogwood trees weekly for the presence of fresh pupal exuviae. Bergh and Leskey (2002) counted dogwood borer males in pheromone traps and collected fresh pupal exuviae from burr knots on apple trees in commercial and experimental orchards in Virginia and West Virginia at weekly intervals from mid-May to mid-October. The same data were collected from two orchards in Virginia in 2002. Trap catch and emergence data from each study were compared using linear regression analysis, with trap catch as the dependent variable. Data from New York apple orchards (Riedl et al. 1985) showed a good relationship between pupal exuviae or adult emergence and trap catch in 2 of 3 years (Table 2). In Ontario, adult emergence was an even stronger predictor of trap catch in apple orchards (Warner and Hay 1985). Although counts of both pupal exuvia and trap catch from dogwood stands in Kentucky were bimodal (Eliason and Potter 2000), the relationship between these variables was weak. Similarly, our data from 2001 and 2002 in Virginia and West Virginia apple orchards showed that trap catch and counts of pupal exuvia were related only poorly or not at all. Except for the Darkesville orchard, from which only nine pupal exuvia were found, there were no consistent indications that emergence from apple occurred predominantly during any month from May through August in Virginia or West Virginia (Table 3). Differences in the strength of the relationship between emergence and trap catch developed for studies from northern and more southern locations may be explained in part by differences in the seasonal flight patterns in the respective regions (Table 1). In northern locations, dogwood borer showed a unimodal flight that was shorter in duration than in regions to the south, and the strongest relationship occurred from the study in Ontario where emergence and flight appeared to be most synchronous. In Kentucky, Virginia, and West Virginia, factors that may have contributed variability not explained by the relationship include less synchrony, bimodal flight, the possibility of effects of



Volume 135


621

TABLE 2. Coefficients of determination for the relationship between pupal exuvia or adult abundance and the capture of Synanthedon scitula males in pheromone traps. Relationship (r2) Location Ontario New York

Adult emergence versus trap catch

Pupal exuviae versus trap catch

0.781 0.679

Kentucky Virginia* West Virginia† Virginia*

0.337 0.679 0.197 0.029, 0.001 0.148, 0.319 0.054, 0.149

Researchers and year of research Warner and Hay 1983 Riedl et al. 1982 Riedl et al. 1983 Riedl et al. 1984 Eliason and Potter 2000 Bergh and Leskey 2001 Bergh and Leskey 2001 Bergh and Leskey 2002

* Data from Virginia are based on weekly captures of males in two traps per orchard baited with Scenturion dogwood borer lures and weekly pupal exuvia counts from 31 May to 15 October 2001 and from 3 May to 7 October 2002. Pupal exuviae were collected from the same 20 and 30 trees per orchard in 2001 and 2002, respectively. † Data from West Virginia are based on weekly captures of males in two traps per orchard baited with Trécé lilac borer lures and weekly pupal exuvia counts from the same 12 trees per orchard between 15 May and 9 October 2001.

emergence from different host plants, immigration from outside the orchards, and climatic differences among regions. Another factor that could influence the outcome of comparisons of trap catch with counts of pupal exuvia is the presence of the closely related apple bark borer, Synanthedon pyri (Harris), which has long been considered a minor pest of apple in eastern North America (Woodside 1952; Dean 1969). Apple bark borer and dogwood borer infest the same sites on apple trees (Woodside 1952), including burr knots (Warner and Hay 1985). Larvae, pupal exuvia, and adults of S. pyri and S. scitula are similar in appearance (Woodside 1952), and Underhill (1935) mentioned the potential for confusing the two species in collections of clearwing borers from apple. Distinguishing adults of these species, however, is aided by the presence of a distinct, orange discal mark and a wedge-shaped anal tuft on S. pyri (Taft et al. 1991). Furthermore, these species purportedly use different compounds in their sex pheromone (Taft et al. 1991). Riedl et al. (1985) captured several species of clearwing moths in pheromone traps deployed for dogwood borer in New York but did not report capturing S. pyri. Warner and Hay (1985) collected both species from apple orchards in Ontario but concluded that dogwood borer was the main species infesting apple burr knots. Recent surveys of borers in apple (Kain and Straub 2001) did not report the presence of S. pyri, and its prevalence remains unknown. Trap placement appears to be important in monitoring dogwood borer. In an orchard with 2.7 m tall apple trees, Riedl et al. (1985) captured significantly greater numbers of dogwood borer males in pheromone traps placed at 1.2 m than at 0.7 or 2.4 m. The 1.2-m height remains the recommended position in the canopy for traps deployed to monitor dogwood borer flight in apple (Hogmire 1995). Dogwood borer sex attractant Perhaps most importantly, the effectiveness of the attractant used also affects the ability of pheromone traps to accurately reflect seasonal patterns of emergence and flight or population density. Tumlinson et al. (1974) isolated the first Sesiidae sex pheromones, reporting (Z,Z)- and (E,Z)-3,13-octadecadien-1-ol acetate (ODDA) for peachtree borer and lesser peachtree borer, respectively. Trapping and electroantennogram studies



622



TABLE 3. Percentage of Synanthedon scitula pupal exuviae collected, by month, from apple trees in Virginia and West Virginia orchards. West Virginia†

Virginia* Cedar Creek Grade

Buffalo Marsh Road

Kearneysville

Darkesville

2001 (n = 43)

2002 (n = 122)

2001 (n = 49)

2002 (n = 139)

2001 (n = 49)

2001 (n = 9)

28 21 16 19 14 2

13 43 20 16 7 1

10 34 31 21 2 2

11 21 27 35 6 0

6 20 39 24 10 0

0 0 67 22 11 0

May June July August September October

NOTE: Fresh pupal exuviae were collected weekly from the same trees in each orchard. * Twenty and 30 trees per orchard were used in 2001 and 2002, respectively. † Twelve trees per orchard were used in 2001.

using these compounds alone, in binary combinations, and in combination with other geometrical isomers and corresponding alcohols revealed that many species of clearwing moths use isomers of 3,13-ODDA in their sex pheromone (Tumlinson 1979; Nielsen et al. 1979). Nielsen et al. (1975, 1979) showed that (Z,Z)-3,13-ODDA is an attractant for dogwood borer males. Several authors have reported a reduced response of dogwood borer males to (Z,Z)-3,13-ODDA when small amounts of other isomers or the corresponding alcohol ((Z,Z)-3,13-ODDOH) were added to the blend, although this effect has not been consistent among studies. Karandinos et al. (1977) and Greenfield and Karandinos (1979) concluded that the response of dogwood borer to (Z,Z)-3,13ODDA was reduced by the addition of (E,Z)-3,13-ODDA. Conversely, Snow et al. (1985) reported that similar numbers of dogwood borer males were captured in pheromone traps baited with either a 96:4 blend of (Z,Z)-3,13-ODDA to (E,Z)-3,13-ODDA (peachtree borer pheromone) (Nielson et al. 1975; Barry et al. 1978) or a 99% pure (Z,Z)-3,13-ODDA formulation, although addition of either (Z,Z)-3,13-ODDOH or (E,Z)-3,13-ODDOH in a 1:1 ratio with the 96:4 blend of (Z,Z)-3,13-ODDA to (E,Z)3,13-ODDA reduced the capture substantially. Warner and Hay (1985) found that traps with peachtree borer pheromone captured dogwood borer males when deployed alone, but when deployed simultaneously with traps containing 99+% (Z,Z)-3,13-ODDA, the capture of dogwood borer males in traps with peachtree borer pheromone was eliminated. Snow et al. (1989) reported that a 50:50 blend of (Z,Z)-3,13-ODDA and (Z,Z)2,13-ODDA was as attractive as (Z,Z)-3,13-ODDA alone. Alm et al. (1989) anecdotally reported capturing dogwood borer males in traps baited with grape root borer, Vitacea polistiformis (Harris) (Lepidoptera: Sesiidae), sex pheromone, a 99:1 blend of (E,Z)2,13-ODDA and (Z,Z)-3,13-ODDA (Snow et al. 1987). Similarly, Snow et al. (1991) reported that dogwood borer males were captured in traps with grape root borer pheromone in 10 of 13 states. Although relatively few moths were captured in nine states, nearly 600 dogwood borer males were trapped in South Carolina. Regardless of the varied results from the aforementioned studies, the consensus appears to remain that (Z,Z)3,13-ODDA is the attractant of choice for trapping dogwood borer and recent studies have relied on commercial lures presumably containing that compound (Pfeiffer and Killian 1999) or lures known to contain the pure compound (Eliason and Potter 2000).



Volume 135


623

Commercial pheromone lures According to Tumlinson (1979), producing isomers of 3,13-ODDA in greater than 99% purity is a difficult, laborious, and costly process. Furthermore, batches of commercial pheromone lures may vary in concentration or purity of ODDA isomers (Barry et al. 1978). Consequently, pheromone lures marketed for trapping particular species of Sesiidae moths tend to be somewhat generic and often catch males from a number of species. In Maryland, lures for peachtree borer and lilac/ash borer, Podosesia syringae (Harris) (Lepidoptera: Sesiidae), from Trécé (Trécé Inc, Salinas, California) and for clearwing borers and dogwood borer from Scentry (Scentry Inc, Billings, Montana) captured between five and seven species belonging to three genera (Braxton and Raupp 1995). Pfeiffer and Killian (1999) captured seven species in traps baited with Trécé lilac borer or dogwood borer lures deployed in a Virginia apple orchard. The use of pure (Z,Z)-3,13-ODDA also results in cross-species attraction. Using this compound, Rogers and Grant (1990) captured eight species of clearwing borers in several habitats in Tennessee. Several studies have reported qualitative or quantitative differences in the relative effectiveness of commercial attractants used to monitor dogwood borer. Based on work in Maryland, Davidson et al. (1992) and Braxton and Raupp (1995) concluded that commercially available pheromone lures for dogwood borer are not reliable for monitoring adult flight activity. Riedl et al. (1985) mentioned that dogwood borer were captured in traps baited with peachtree borer lures from Pherocon (Trécé Inc, Salinas, California), but that Scentry clearwing borer lures were more effective. Braxton and Raupp (1995) suggested that more dogwood borer were captured in Maryland by the Trécé lilac/ash borer lure than by the Scentry dogwood borer lure. Pfeiffer and Killian (1999) reported that the Trécé lilac borer lure captured significantly more dogwood borer males than the Trécé dogwood borer lure in Virginia and this observation was independently confirmed in West Virginia in 2000 (HW Hogmire, personal communication). Bergh and Leskey (2002) found that the Scenturion (Scenturion Inc, Clinton, Washington) dogwood borer lure was significantly more attractive than the Trécé lilac borer lure in Virginia apple orchards and that results from comparisons of the Trécé lilac borer and dogwood borer lures in West Virginia were inconsistent. Subsequently, Bergh and Leskey (2003) compared four commercially available lures (Trécé lilac borer and dogwood borer, Scentry dogwood borer, and Scenturion dogwood borer) in five apple orchards in Virginia and West Virginia. Traps baited with the Scenturion dogwood borer lure captured significantly more dogwood borer males in three orchards and numerically more at all five locations. As well as being most attractive to dogwood borer, the Scenturion lure was also the most selective lure tested, capturing the fewest peachtree and lesser peachtree borers at all sites. Despite its apparent superiority, the Scenturion lure does not appear to accurately reflect the emergence or population density of dogwood borer. Leskey and Bergh (2003) reported a method for differentiating male and female dogwood borer pupae and pupal exuviae based on the number of rows of posteriorly projecting spines on the fused, terminal abdominal segments; males and females have three and four rows, respectively. This method has enabled the measurement of temporal changes in the relative number of adults of each sex in the population. Bergh and Leskey (2003) compared the cumulative number of fresh male and female pupal exuviae collected from burr knots at weekly intervals from early May through mid-June at two commercial orchards in Virginia with the cumulative capture of dogwood borer males in traps baited with Scenturion lures. Protandry of dogwood borer was indicated at both locations and more male than female pupal exuviae were collected each week through late May at one orchard and through mid-June at the other. Despite the fact that pupal exuvia were



624



collected from only 30 trees per orchard in orchards that were nearly 5 ha in size, the cumulative number of male pupal exuviae exceeded the cumulative number of moths captured in traps. This finding suggests that the lures were suboptimal in their attractiveness and did not compete well with calling virgin female moths. Clearly, the confusion and discrepancies surrounding the monitoring of dogwood borer with sex attractants in apple orchards and other habitats has been due to the use of compounds and blends of compounds that have not been specifically isolated from the effluvia or pheromone gland of calling dogwood borer females.

Developmental rate and voltinism The geographical range of dogwood borer encompasses the eastern half of the United States of America and southeastern Canada (Eichlin and Duckworth 1988). In the eastern apple growing regions of North America, dogwood borer has also been recorded from numerous other host plants (Howitt 1993). To date, only limited data on the developmental rate of dogwood borer have been reported, based exclusively on individuals collected from or reared on dogwood. Although Underhill (1935) stated that data on the number of generations and the developmental period of dogwood borer were not complete, he reported that it is univoltine in Virginia. Despite pronounced differences in the duration of emergence and flight, the number of flight peaks (Table 1), and climatic conditions among regions within its range, most subsequent reports on dogwood borer have reiterated the conclusion of univoltinism, although Snow et al. (1985) suggested that it may be multivoltine in Georgia. Two studies reported a similar developmental duration of dogwood borer eggs, averaging 8–9 d (Underhill 1935; Pless and Stanley 1967) (Table 4). Wallace (1945) reported six larval instars of dogwood borer, using head-capsule measurements from 47 individuals. Ayers (1966) found seven larval instars, based on a much larger sample, and Neal (1984) concurred that Wallace (1945) had overlooked the first larval instar. Underhill (1935) provided the only data on the developmental duration of dogwood borer larvae, although environmental conditions were not reported. Between late August and late October, 22 larvae that provided blocks of dogwood for food showed larval instar durations ranging in length from 8 to 50 d and averaging 17.5 d. Pless and Stanley (1967) reported that individual larvae fed on the cambium and phloem layers of dogwood for about 12 months, although no data were provided. Despite the lack of details about experimental conditions, the average duration of the prepupal and pupal stages was similar among three reports (Underhill 1935; Wallace 1945; Pless and Stanley 1967) (Table 4). Based on the information available, Pless and Stanley (1967) provided diagrammatic representations of the annual cycle of dogwood borer populations and the phenology of individuals in dogwood. Riedl et al. (1985) caged the trunk of 20 infested apple trees in the spring of 1983, prior to adult emergence, mating, and oviposition and left them in place for 2 years. Sixty-four dogwood borer were recovered in 1983 and four in 1984, leading them to suggest that some larvae may require 2 years to complete development. Riedl et al. (1985), however, did caution that more data would be necessary to confirm this conclusion. From April 2002 to April 2003, we collected dogwood borer from burr knots cut from the rootstock of 10 trees in each of two commercial apple orchards in Virginia and two in West Virginia. Samples were taken at approximately monthly intervals from spring through fall and less frequently thereafter. The burr-knot tissue removed from each tree was examined for all juvenile stages of dogwood borer, including unhatched eggs, using a dissecting microscope. The head capsule of all larvae found was measured



Dogwood

Dogwood Dogwood

Virginia

Connecticut Tennessee

— 2

—

n

Egg

8.5

8–9

Duration (d)*

About 27°C

Mid-July

Condition†

32

n

6.6

Insectary

Condition†

Prepupa Duration (d)* 7 33 32 — —

n

NOTE: —, information was not provided. Values in parentheses are the duration of the prepupa plus pupal stage in column 10. * Developmental durations are averages. † Conditions are those provided in Underhill (1935), Wallace (1945), and Pless and Stanley (1967).

Host plant

Pupa

(18.4) (18.9) 12.4 (20) 10

Duration (d)*

— — Insectary — July

Condition†

Wallace 1945 Pless and Stanley 1967

Underhill 1935

Reference

Volume 135

Location

TABLE 4. Reported developmental durations for life stages of Synanthedon scitula.



625


626



at its widest point and determinations of larval instar were based on the measurements of Ayers (1966). Dogwood borer does not have an obligatory diapause and can resume feeding and development during warm periods in the winter (Wallace 1945; Pless and Stanley 1967; Potter and Timmons 1983). Riedl et al. (1985) reported that instars four through six constituted 59.4% of overwintering larvae collected in April from apple trees in New York, although their measurements were based on those of Wallace (1945) (i.e., six instars). In 2002, the overwintering population sampled in late April and early May in Virginia and West Virginia consisted primarily of larval instars five through seven (Table 5). In April 2003, larval instars five through seven represented a smaller percentage of the overwintering population (Table 5). This was probably due largely to the much colder winter in 2002–2003 than in the previous year and its effect on the amount of larval feeding and development that occurred during the fall and winter. Because dogwood borer does not overwinter as a pupa and pupae are generally not found after the first week of October (Underhill 1935; Pless and Stanley 1967), pupation of those collected in late April presumably occurred earlier that month (Table 5). Emergence and mating of adults during May was indicated by the presence of pupal exuviae and unhatched eggs in the samples taken in late May and early June. By late June, the eclosion and development of larvae from eggs deposited during the spring was indicated by the presence of greater numbers of instars one through four. From late June through late August, all larval instars were found, pupae and pupal exuviae were collected, and the number of trees with unhatched eggs peaked between late July and late August (Table 5). The number of fresh pupal exuviae collected declined in September and October (Table 3), concurring with previous observations (Underhill 1935; Pless and Stanley 1967), and egg deposition appeared to end between late August and late September. In combination with our emergence data based on collections of fresh pupal exuviae (Table 3), our data on the seasonal changes in the distribution of larval instars raise questions about the voltinism and bimodal flight of dogwood borer that develop on apple burr-knot tissue in the mid-Atlantic region. A substantial percentage (range 23–41%) (Table 3) of the total number of fresh pupal exuviae were found from August to September, whereas 86–100% of the overwintering larval population collected in 2002 consisted of instars five through seven in late April (Table 5). If most overwintering larvae complete development and emerge as adults by early July, forming the first flight peak, then the second flight peak in late summer may be composed, at least in part, of individuals that emerge in the spring and complete development by late summer. Given a temperature-dependent developmental rate, larval development would occur most rapidly during the warmest months from June through September. In this case, dogwood borer would be considered bivoltine in this region. In the alternative scenario, the first peak of flight likely consists mainly of individuals that eclosed from eggs deposited the previous spring and the second peak of those deposited the previous summer, in which case dogwood borer would be considered univoltine; however, dogwood borer larvae may develop more rapidly in apple burr knots than in other apple tissue. In southern Germany, the apple clearwing moth, S. myopaeformis, has a 2-year life cycle when it develops in the bark of the trunk or branches of apple trees but completes development in 1 year when feeding in burr knots (Dickler 1976). The duration of emergence of S. myopaeformis, however, is considerably shorter in southern Germany (late June though early August) (Dickler 1976) than that of dogwood borer in the midAtlantic region. Without definitive data comparing the rate of development of dogwood borer larvae on different host-plant tissues and (or) under defined experimental conditions, the conclusion of univoltinism in much of its geographical range remains equivocal.



27 30 27 29 28 25 29 17 25 24

6 2 2 30 27 1 23 21 19 23

Virginia

West Virginia

0 0 2 1 1 2 0 0 0 0

0 0 4 4 9 2 8 1 1 1

2

4 0 11 2 4 2 9 0 1 9

0 0 6 4 8 6 16 4 2 2

3

1 0 4 2 0 3 3 0 0 3

0 0 0 2 5 2 1 2 1 5

4

23 2 10 1 6 6 5 2 2 6

11 3 0 6 12 9 14 5 2 11

5

6 4 0 5 3 1 4 1 1 1

10 2 1 7 5 3 4 8 1 0

6

8 9 10 6 4 4 15 3 1 5

17 10 6 8 1 16 32 8 6 5

7

1 8 2 4 4 0 0 0 0 0

15 12 8 9 11‡ 0 8‡ 0 0 1

Pupae†

1 1 6 2 4 5 3 0 2 0

0 5 28 13 15 0 0 0 0 0

Pupal exuviae

0 5 4 7 3 0 0 0 0 0

0 1 7 6 12 4 0 0 0 4

Eggs


* Samples are based on pooled data from 10 trees per orchard from orchards in Virginia (Cedar Creek Grade and Buffalo Marsh Road) and West Virginia (Kearneysville and Arden). † Data from Virginia include both pupae and prepupae (i.e., larvae in pupal chamber), whereas data from West Virginia include pupae only. ‡ Seven pupae or prepupae and 8 prepupae found in Virginia on 28 August and 29 October, respectively, were parasitized.

1 0 3 2 0 0 0 0 0 0

0 0 4 0 9 0 0 0 0 0

1

Volume 135

May 2002 June 2002 July 2002 July 2002 August 2002 October 2002 October 2002 January 2003 March 2003 April 2003

April 2002 May 2002 June 2002 July 2002 August 2002 September 2002 October 2002 December 2002 March 2003 April 2003

Date

Location

Instar

Number of dogwood borer larvae, pupae, and pupal exuviae from 20 trees, and number of trees with unhatched eggs*

TABLE 5. Distribution of developmental stages of Synanthedon scitula collected at intervals from burr knots on apple trees in commercial orchards in Virginia and West Virginia.


627


628



Control strategies in apple A survey of 33 apple orchards in western New York revealed that about one-third of the trees grown on clonal rootstocks from the Malling (M) and Malling–Merton (MM) series were infested by dogwood borer (Riedl et al. 1985). Infestation levels among orchard blocks ranged from 0 to 100%. Trees on M.9, M.26, MM.106, and M.9 interstem on MM.106 were equally infested, whereas those on MM.111 showed significantly lower infestation levels. There was not a significant effect of rootstock on the percentage of trees with burr knots or on the number of burr knots per tree, and the factor underlying the lower infestation of trees on the MM.111 rootstock was not apparent (Riedl et al. 1985). ‘MacIntosh’ on M.26, ‘Golden Delicious’ on M.9, and ‘Ida Red’ on MM.106 showed the highest infestation levels (76–85% of trees surveyed). Howitt (1993) surmised that the susceptibility of ‘Empire’ to attack by dogwood borer is due to the large number of burr knots produced by that variety. In southern Germany, apple trees planted on M.9 rootstock showed varietal differences in the degree of infestation by S. myopaeformis. ‘Mutsu’ was most heavily infested (70.6%), followed by ‘Maigold’ and ‘Ida Red’ (51–56%), whereas ‘Granny Smith’ showed relatively low levels of infestation (20%) (Dickler 1976). A recent survey by Kain and Straub (2001) was prompted by reports that infestation of burr knots on dwarf apple trees by the American plum borer, Euzophera semifuneralis (Walker) (Lepidoptera: Pyralidae), and dogwood borer were increasing in frequency in the northeastern United States of America. Kain and Straub (2001) found that dogwood borer was the most prevalent pest in apple blocks isolated from stone fruit orchards, but that American plum borer could also be problematic in blocks near cultivated or wild cherry, Prunus sp. L. (Rosaceae), peach, Prunus persica L. (Rosaceae), or stumps of those trees. Howitt (1993) stated that apple trees can show a slow decline and reduced yield in response to several years of continued infestation by dogwood borer larvae, although there are no reports from North America quantifying the effect. In Europe, infestation of ‘Ida Red’ trees by S. myopaeformis over a period of 2 years resulted in a 22.1% decline in yield (Dickler 1976). Given the positive relationship between the height of the graft union above the soil and the number of burr knots on the rootstock (Riedl et al. 1985; Warner and Hay 1985), cultural practices that reduce the number or exposure of burr knots can help reduce infestation by dogwood borer. Young and Tyler (1983) showed that mounding soil around the exposed rootstock promoted the development of roots from burr knots and Riedl et al. (1985) reported that burying rootstocks with infested burr knots prevented the emergence of dogwood borer adults and further infestation of them. The longevity of mounding, however, may vary according to the slope of an orchard, soil type, and the effects of erosion from run-off of rain. Application of napthalene acetic acid (NAA) to exposed rootstocks destroyed burr knots, although did not prevent further attacks by dogwood borer (Riedl et al. 1985). Riedl et al. (1985) cautioned that this practice could result in more significant damage by causing larvae to mine outward from dead burr knots into healthy cambium tissue. Reducing exposed burr knots by planting new apple trees more deeply also has been recommended (Young and Tyler 1983; Riedl et al. 1985; Warner and Hay 1985; Kain and Straub 2001), although the potential for adverse horticultural effects from rooting of the scion must be considered (Riedl et al. 1985; Kain and Straub 2001). Furthermore, planting trees deeply in poorly drained soil is not recommended, and planting depth is influenced by the height of the graft union above the nursery roots (Young and Tyler 1983). To eliminate exposed burr knots and avoid the potential negative effects of deep planting, Young and Tyler (1983) recommended that apple trees propagated on clonal rootstocks should be grafted no higher than 20– 25 cm above the nursery roots. Mounding soil around the rootstock or planting new



Volume 135


629

trees deeply does not entirely resolve the problem of dogwood borer infestation of burr knots. Some varieties of apple propagated on clonal rootstocks tend to produce burr knots on the trunk and scaffold limbs, and these are also subject to infestation by dogwood borer (Howitt 1993; Pfeiffer and Killian 1999). Weed control around the trunk is recommended to reduce shade and humidity, as these factors also promote development of burr knots (Howitt 1993; Kain and Straub 2001). Similarly, tree guards used for protection from gnawing by rabbits and rodents enhance the growth of burr knots (Rom and Brown 1979) and can increase the severity of infestation by dogwood borer and American plum borer (Kain and Straub 2001). This is especially true of the tightly wrapped, plastic, spiral guards (Kain and Straub 2001) that may protect eggs and larvae from predation or parasitism and create optimal conditions for their development, probably decrease the penetration of trunk drench insecticide applications and certainly hide a developing infestation from view. Vinyl tree wraps have also been shown to increase the likelihood and severity of dogwood borer infestation of ornamental dogwood trees in managed landscapes (Owen et al. 1991). Of the pesticides available for managing dogwood borer in apple, trunk drench applications of chlorpyrifos have provided the most consistent and greatest control (Riedl et al. 1985; Kain and Straub 2001; Kain et al. 2002, 2003). A single application of chlorpyrifos in June, at the beginning or peak of egg-hatch, provided season-long control in New York (Riedl et al. 1985). Kain and Straub (2001) showed that single applications of chlorpyrifos at petal-fall or mid-season were equally effective and as effective as two applications. The duration of the residual effect of chlorpyrifos on dogwood borer control in apple remains uncertain. Although prebloom treatments appeared to lose some residual activity by mid-July, compared with sprays applied at petal-fall (Kain et al. 2002), postharvest applications controlled overwintering larvae and may have suppressed infestations through the following growing season (Kain et al. 2003). The residual effect of prebloom applications appeared to be prolonged by combining chlorpyrifos with diluted, white latex paint (Kain et al. 2002). Ongoing regulatory and registration changes driven by the Food Quality Protection Act make the long-term availability of chlorpyrifos and other organophosphate pesticides in the United States of America uncertain (Kain and Straub 2001). This has prompted evaluation of the efficacy of other materials against dogwood borer, although to date, none are considered as effective as chlorpyrifos. Undiluted, white latex paint brushed on burr knots has been effective in some tests on apple (Riedl et al. 1985; Warner and Hay 1985), but less so in others (Kain and Straub 2001). Two or three applications of endosulfan, indoxacarb, and fenpropathrin showed intermediate levels of activity compared with a single application of chlorpyrifos (Kain et al. 2002, 2003). Single sprays of the neonicotinoids thiamethoxam and thiachloprid at peak flight of dogwood borer in Michigan reduced larval populations to levels comparable to chlorpyrifos, although the degree of toxicity and the length of residual control were unclear (Wise and Gut 2002). Materials that did not control dogwood borer infestation in apple trials include methoxyfenozide and kaolin clay (Kain et al. 2003). Research on options for biological control of dogwood borer remains limited. Entomopathogenic nematodes have shown promise for control of some clearwing borer pests of currants (Miller and Bedding 1982), ornamental trees (Kaya and Brown 1986), and grapevines (Williams et al. 2002). In studies on clearwing pests of ornamental trees, Steinernema carpocapsae (Weiser) (Rhabditida: Steinernematidae) was efficacious against Synanthedon culiciformis L. in alder (Alnus sp. Mill. (Betulaceae)) and Synanthedon resplendens Hy. Edwards in sycamore (Platanus sp. L. (Platanaceae)) (Kaya and Brown 1986). In the sole report on the use of nematodes for dogwood borer control, Davidson et al. (1992) reported that applications of Ste. carpocapsae to nursery



630



dogwood trees infested with dogwood borer reduced the number of trees with larvae and significantly reduced the number of larvae per tree. Numerous species of arthropod natural enemies have been collected from dogwood borer larvae and pupae, although there are no reports of the effect of predation or parasitism on the population dynamics of dogwood borer. Apanteles sesiae Vier. (Hymenoptera: Braconidae) was most commonly collected from larvae by Underhill (1935) and also reported by Potter and Timmons (1983). Other Braconidae reared from larvae collected from dogwood include Microbracon sanninoideae Gahan and Microbracon mellitor Say (Underhill 1935) and Agathis buttricki Vier. (Pless and Stanley 1967). In Connecticut, Wallace (1945) found that larvae of an unidentified species (Coleoptera: Cleridae) were common and were observed feeding on dogwood borer larvae. Parasitoids (Hymenoptera: Ichneumonidae) collected from pupae include Phaeogenus ater (Cress.), Scambus conquisitor Say (Underhill 1935), and Ichneumon irritator Fabr. (Wallace 1945). Two gregarious species of wasps have been collected from dogwood borer pupae. Elachertus sp. (Hymenoptera: Eulophidae) emerged from pupae collected from dogwood in Kentucky (Potter and Timmons 1983). In Virginia, Hyssopus sanninoideae (Gir.) (Hymenoptera: Eulophidae) was found in pupae from dogwood (Underhill 1935) and we have found H. sanninoideae in pupae taken from trees in commercial apple orchards in Virginia and West Virginia. The percentage of parasitized pupae and prepupae appears to increase late in the growing season (Table 5), but levels of parasitism have not, in our experience, been of sufficient magnitude to reduce damage by larvae. Underhill (1935) mentioned that up to 50% of dogwood borer larvae collected from flowering dogwood trees were parasitized by A. sesiae, although the effectiveness of arthropod natural enemies of dogwood borer in apple is probably adversely affected by frequent insecticide applications. Alternative management options for dogwood borer based on behavioral manipulation, including mating disruption and attract and kill, may offer considerable potential. The capture of males of the congeneric species peachtree borer and lesser peachtree borer in pheromone traps has been nearly or completely eliminated in orchards permeated with (Z,Z)-3,13-ODDA (Gentry et al. 1980; Snow et al. 1985). Using the lesser peachtree borer pheromone (E,Z)-3,13-ODDA, Pfeiffer et al. (1991) reported complete disruption of trap catch and reduced infestation levels of lesser peachtree borer in disrupted orchards relative to those treated with pesticides, although the reduction of infestation was not as pronounced as was the disruption of trap catch. In the only published dogwood borer mating disruption trial, Pfeiffer and Killian (1999) deployed Isomate-P (peachtree borer) (Shin-Etsu Fine Chemical Co, Tokyo, Japan) pheromone dispensers (96:4 blend of (Z,Z)-3,13-ODDA to (E,Z)-3,13-ODDA) in 2-ha plots of ‘Gala’ apples in Virginia. Capture of male dogwood borer in pheromone traps was reduced by nearly 100% in 3 consecutive years, although the percentage of burr knots with dogwood borer larvae, pupal exuviae, or fresh frass was not reduced compared with conventionally managed blocks. Attract-and-kill pest management technology combines a long-distance olfactory stimulus with a killing agent and (or) collection device (Foster and Harris 1997). Formulations combining sex pheromone and permethrin have been used successfully to control codling moth (Charmillot et al. 2000; Larsen and Smith 2001) and light brown apple moth, Epiphyas postvittanna (Saunders) (Lepidoptera: Tortricidae) (Suckling and Brockerhoff 1999), in apple. The use of Sesiidae sex pheromones toward this end has not been reported. Host-plant volatiles used by phytophagous insects for location and selection of food, mates, and (or) oviposition sites (Visser 1986; Bernays and Chapman 1994) are another potential source of olfactory stimuli for use in attract-and-kill technology and the identification of such volatiles is an important emerging area in insect pest management (Averill et al. 1988; Zhang et al. 1999; Light et al. 2001). Given the



Volume 135


631

behavioral responses to wounded host-plant tissue demonstrated for several Sesiidae pests of conifers and deciduous fruit trees, the use of host-plant volatiles as attractants for female moths may be a viable alternative for some species of clearwing borers. Wounded areas on the trunk of Monterey pine trees, Pinus radiata D. Don (Pinaceae), showed increased levels of infestation by the sequoia pitch moth, Synanthedon sequoiae (Hy. Edwards) (Koehler et al. 1983). Female Douglas-fir pitch moths, Synanthedon novaroensis (Hy. Edwards), were attracted to pruning wounds on Douglas-fir, Pseudotsuga menziesii (Mirb.) Franco (Pinaceae), in Washington State (Johnson 1993). In western Canada, attacks of lodgepole pine, Pinus contorta Engelm, by S. novaroensis were positively related to attacks in previous years (Rocchini 1997), leading Rocchini et al. (2000) to suggest that female moths orient to pitch exuding from wounds. Similar responses have been recorded for the peach pests, S. exitiosa and S. pictipes. Gentry and Wells (1982) found that filter-paper wicks treated with solvent extracts of cocoons, peach tree bark, frass, and peach gum mixtures stimulated oviposition by caged, gravid peachtree borer females. Reed et al. (1988) reported that mated lesser peachtree borer females responded to and oviposited on substrates that had been treated with aqueous mixtures of peach bark and canker material. Furthermore, observations in a wind tunnel and in a greenhouse indicated that these volatiles appeared to attract lesser peachtree borer females over distances of several metres (Reed et al. 1988). Electroantennogram bioassays using fractionated peach bark volatiles showed that lesser peachtree borer females responded to active fractions that contained simple aromatic compounds and volatile aliphatic acids and aldehydes. There is strong evidence that mated female dogwood borer are attracted to stimuli associated with wounded host-plant tissue. Dogwood borer infestations of dogwood are generally associated with wounded bark, pruning cuts, or gall tissue (Underhill 1935; Pierce and Nickels 1941; Wallace 1945; Pless and Stanley 1967). Wallace (1945) demonstrated that dogwood borer larvae require wound sites in bark to establish successfully and females likely choose oviposition sites based on proximity to these potential larval feeding sites. Potter and Timmons (1981) examined the factors that predispose flowering dogwood to attack by dogwood borer and showed that the severity of mechanical wounding of the trunk was one of the strongest predictors of infestation. Dogwood borer is one of the most abundant inquilines in horned oak galls formed on pin oak, Quercus palustris Muenchhausen (Fagaceae), by Callirhytis cornigera (Osten Sacken) (Hymenoptera: Cynipidae) (Eliason and Potter 2000). Eliason and Potter (2000) suggested that mated female dogwood borer may orient to volatile emissions from growing galls or galls in which other inhabitants are currently developing. Similar to the scenario suggested by Eliason and Potter (2000), burr knots on apple trees and perhaps even more so, burr knots infested by borer larvae, may emit behaviorally active volatiles to which mated female dogwood borer orient.

Summary discussion There remains much to learn about the life history, behavior, and ecology of dogwood borer in apple and other hosts that directly affects our ability to develop alternative management tactics for it. A major impediment to furthering some key areas of basic and applied research on dogwood borer has been the lack of a sustainable rearing methodology. Several attempts to mate dogwood borer in captivity have been unsuccessful (Underhill 1935; Wallace 1945; Pless and Stanley 1967), but Leskey and Bergh (2002) have recently defined the conditions necessary to mate them in the laboratory. Mated females have oviposited in cups with synthetic, general lepidopteran diet (BioServ, Frenchtown, New Jersey); larvae eclosed from eggs, fed, and developed on such diet and on pieces of carrot. Field-collected larvae have also completed development on



632



the lepidopteran diet. A methodology for culturing dogwood borer should significantly increase our ability to work with this species and we suggest that the following areas are of immediate relevance. As suggested by Tumlinson (1979) and Pfeiffer and Killian (1999), isolation and identification of the dogwood borer sex pheromone is imperative. Even though the Scenturion dogwood borer lure captured more male moths than the others we have tested, it does not appear to compete well with virgin females in the population. Between 30 and 31 July 2001, we captured 19 male moths in a trap baited with a caged, virgin female dogwood borer, but only an average of 7.5 males (range = 7–8) in two traps baited with Scenturion dogwood borer lures during the same period in the same orchard. Field and flight tunnel comparisons of the behavioral response of males to naturally derived pheromone, blends of isomers of 3,13-ODDA and 2,13-ODDA, commercial pheromone lures, and pheromone source concentration should enable the refinement of monitoring through improved attractiveness, competitiveness, and specificity of lures. Such information should help clarify the discrepancies among reports of differences in the relative attractiveness of commercially available lures and further illuminate the role of chemical communication in the reproductive isolation of dogwood borer and sympatric species. An optimized, pheromone-based monitoring system would enable standardized comparisons of seasonal flight activity and emergence patterns among geographical locations and habitats, and would be instrumental in the development of treatment thresholds based on the relationship between trap captures and larval density. Mating-disruption research on dogwood borer would be assisted greatly by using the correct pheromone blend as the disruptant and through improved confidence in the ability of traps to accurately reflect the effect of pheromone treatments. Similarly, lures that compete effectively with virgin female moths are requisite in the development of a pheromone-based attract-and-kill management approach (Krupke et al. 2002). Access to cohorts of virgin and mated female dogwood borer would enable characterization of semiochemicals that elicit orientation and oviposition responses by females to wounded tissue on host plants, and such olfactory stimuli could also be useful in the development of attract-and-kill technology. Given that bimodal flight implies an underlying phenological pattern, the bimodal flight of dogwood borer reported from many locations needs to be reconciled with their development and voltinism in different host plants and under different environmental conditions. With respect to apple, developmental rate studies at constant and ambient temperatures should be conducted with larvae of different instars collected from burrknot tissue at intervals during the growing season. Determination of larval instar should be based on the head-capsule measurements of Ayers (1966), and not Wallace (1945). Information on the effect of environmental cues, particularly day length, on triggering and (or) inhibiting pupation, in combination with the aforementioned developmental rate studies should reveal much about the number of annual generations possible. Studies comparing developmental rates on tissue from different host plants would yield important information on how and when emergence from non-apple hosts may affect immigration into apple orchards by male and female moths and to what degree this might affect the success of mating disruption or attract-and-kill tactics. In all subsequent field research in areas where the sympatric species S. pyri occurs, attention should be given to correct identification and separation of the two species. The importance of dogwood borer as an indirect pest of apple will likely continue to increase as more orchards are planted on size-controlling rootstocks, and its pest status could become even more critical if the insecticides currently used to control it become unavailable or further restricted. Therefore, basic questions regarding its biology, ecology, and behavior must be addressed from the perspective of their importance to the development of behaviorally based alternative management strategies such as mating



Volume 135


633

disruption and attract-and-kill. This effort will be especially important as integrated pest management tactics and alternative tree fruit production systems that are less reliant on synthetic insecticides become more widely adopted (Cross and Dickler 1994; Brown 1999).

References Alm SR, Williams RN, Pavuk DM, Snow JW, Heinlein MA. 1989. Distribution and seasonal flight activity of male grape root borers (Lepidoptera: Sesiidae) in Ohio. Journal of Economic Entomology 82: 1604–8 Averill AL, Reissig WH, Roelofs WL. 1988. Specificity of olfactory responses in the teprhitid fruit fly, Rhagoletis pomonella. Entomologia Experimentalis et Applicata 47: 211–22 Ayers GS. 1966. The bionomics of the dogwood borer, Thamnosphecia scitula (Harris), attacking blueberry in Michigan. MSc thesis, Michigan State University, Ann Arbor. Barry MW, Nielsen DG, Purrington FF, Tumlinson JH. 1978. Attractancy of pheromone blends to male peachtree borer, Synanthedon exitiosa. Environmental Entomology 7: 1–3 Bergh JC, Leskey TC. 2002. Dogwood borer field studies: preliminary data on seasonal phenology, monitoring and voltinism in Virginia and West Virginia. pp 23–30 in PW Shearer (Ed), Proceedings of the 77th Annual Cumberland—Shenandoah Fruit Workers Conference, Winchester, Virginia, 15–16 November 2001. Winchester, Virginia: Cumberland–Shenandoah Fruit Workers ——— 2003. Refining the pheromone based monitoring system for dogwood borer. pp 69–75 in JC Bergh (Ed), Proceedings of the 78th Annual Cumberland–Shenandoah Fruit Workers Conference, Winchester, Virginia, 5–6 December 2002. Winchester, Virginia: Cumberland–Shenandoah Fruit Workers Bernays EA, Chapman RF. 1994. Host–plant selection by phytophagous insects. New York: Chapman and Hall, Inc Braxton SM, Raupp MJ. 1995. An annotated checklist of clearwing borer pests of ornamental plants trapped using commercially available pheromone lures. Journal of Arboriculture 21: 177–80 Brown MW. 1999. Applying principles of community ecology to pest management in orchards. Agriculture, Ecosystems, and Environment 73: 103–6 Charmillot P-J, Hofer D, Pasquier D. 2000. Attract and kill: a new method for control of codling moth Cydia pomonella. Entomologia, Experimentalis et Applicata 94: 211–6 Cross JV, Dickler E. 1994. Guidelines for integrated production of pome fruits. Technical guidelines, III, 2nd edition. International Organization of Biological Control/West Palaearctic Region Section Bulletin 17: 1–12 Davidson JA, Gill SA and Raupp MJ. 1992. Controlling clearwing moths with entomopathogenic nematodes: the dogwood borer case study. Journal of Arboriculture 18: 81–4 Dean RW. 1969. Apple bark borer, Thamnosphecia pyri (Harris). New York Agricultural Experiment Station Bulletin 823: 22–3 Dickler VE. 1976. Zur Biologie und Schadwirkung von Synanthedon myopaeformis Brkh. (Lepid., Aegeriidae), einem neuen Schädling in Apfeldichtpfanzungen. Zeitschrift fuer Angewandte Entomologie 82: 259–66 Eichlin TD, Duckworth WD. 1988. Sesioidea: Sesiidae. pp 1–176 in RB Dominick et al. (Eds), The moths of America north of Mexico. Fascicle 5.1. Washington, District of Columbia: Wedge Entomological Research Foundation Eliason EA, Potter DA. 2000. Dogwood borer (Lepidoptera: Sesiidae) infestation of horned oak galls. Journal of Economic Entomology 93: 757–62 Engelhardt GP. 1932. Business proceedings of the eastern branch of the American Association of Economic Entomologists. Journal of Economic Entomology 25: 293–4 Foster SP, Harris MO. 1997. Behavioral manipulation methods for insect pest management. Annual Review of Entomology 42: 123–46 Gentry CR, Wells JM. 1982. Evidence of an oviposition stimulant for peachtree borer. Journal of Chemical Ecology 8: 1125–32 Gentry CR, Bierl-Leonhardt BA, McLaughlin JR, Plimmer JR. 1980. Air permeation tests with (Z,Z)-3,13octadecadien-1-ol acetate for reduction in trap catch of peachtree and lesser peachtree borer moths. Journal of Chemical Ecology 7: 575–82 Greenfield MD, Karandinos MG. 1979. Reproductive isolation in Sesiidae: a niche analysis approach. pp 67–74 in Pheromones of the Sesiidae. SEA-AR, ARR-NE-6. Washington, District of Columbia: United States Department of Agriculture Herrick GW. 1904. Insects injurious to pecans. Mississippi Agricultural Experiment Station Bulletin 86: 11– 5 Howitt AH. 1993. Common tree fruit pests. Michigan State University, North Central Regional Extension Publication 63



634



Johnson JM. 1993. Flight, emergence, and oviposition patterns of the Douglas-fir pitch moth, Synanthedon novaroensis (Hy. Edwards) (Lepidoptera: Sesiidae), in western Washington. MSc thesis, University of Washington, Seattle Johnson WT, Lyon HH. 1991. Insects that feed on trees and shrubs. 2nd edition. Ithaca, New York: Comstock Press Kain DP, Straub R. 2001. Status of borers infesting apple burr knots and their management in New York orchards. New York Fruit Quarterly 9: 10–2 Kain DP, Straub R, Agnello A. 2002. Apple, evaluation of various trunk sprays to control borers infesting burr knots, 2001. Arthropod Management Tests 27: A42 ——— 2003. Apple, evaluation of various trunk sprays to control borers infesting burr knots, 2002. Arthropod Management Tests. In press Karandinos MG, Tumlinson JH, Eichlin TD. 1977. Field evidence of synergism and inhibition in the Sesiidae sex pheromone system. Journal of Chemical Ecology 3: 57–64 Kaya HK, Brown LR. 1986. Field application of entomogenous nematodes for biological control of clearwing moth borer in alder and sycamore trees. Journal of Arboriculture 12: 150–4 Koehler CS, Frankie GW, Moore WS, Landwehr VR. 1983. Relationship of infestation by the Sequoia pitch moth (Lepidoptera: Sesiidae) to Monterey pine trunk injury. Environmental Entomology 12: 979–81 Krupke CH, Roitberg BD, Judd GJR. 2002. Field and laboratory bioassay of male codling moth (Lepidoptera: Tortricidae) to a pheromone based attract-and-kill strategy. Environmental Entomology 31: 189–97 Larsen M, Smith RF. 2001. Evaluation of last Call for codling moth (CM) management in Maritime apple orchards as an alternative to conventional pesticides. Annual Report to the Nova Scotia Fruit Growers Association 138: 33–41 Leskey TC, Bergh JC. 2002. Rearing methods for the dogwood borer, Synanthedon scitula (Harris). pp 31–32 in PW Shearer (Ed), Proceedings of the 77th Annual Cumberland–Shenandoah Fruit Workers Conference, Winchester, Virginia, 15–16 November 2001. Winchester, Virginia: Cumberland–Shenandoah Fruit Workers ——— 2003. A simple character for sex differentiation of pupae and pupal exuviae of the dogwood borer (Lepidoptera: Sesiidae). Florida Entomologist 86: 379–81 Light DM, Knight AL, Henrick CA, Rajapaska D, Lingren B, Dickens JC, Reynolds KM, Buttery RG, Merrill G, Roitman J, Campbell BC. 2001. A pear-derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.). Naturwissenschaften 88: 333–8 Miller LA, Bedding RA. 1982. Field testing of the insect parasitic nematode, Neoaplectana bibioniz (Nematoda: Steinernematidae) against currant borer moth, Synanthedon tipuliformis (Lep.: Sesiidae) in blackcurrants. Entomophaga 27: 109–4 Neal JW. 1984. Bionomics and instar determination of Syanthedon rhododendri (Lepidoptera: Sesiidae) on rhododenron. Annals of the Entomological Society of America 77: 552–60 Nielsen DG, Purrington FF, Tumlinson JH, Doolittle RE, Yonce CE. 1975. Response of male clearwing moths to caged virgin females, female extracts, and synthetic sex attractants. Environmental Entomology 4: 451–4 Nielsen DG, Purrington FF, Shanbaugh GF. 1979. EAG and field responses of sesiid males to sex pheromones and related compounds. pp 11–26 in Pheromones of the Sesiidae. SEA-AR, ARR-NE-6. Washington, District of Columbia: United States Department of Agriculture Owen NP, Sadof CS, Raupp MJ. 1991. The effect of plastic tree wrap on borer incidence in dogwood. Journal of Arboriculture 17: 29–31 Pfeiffer DG, Killian JC. 1999. Dogwood borer (Lepidoptera: Sesiidae) flight activity and an attempt to control damage in ‘Gala’ apples using mating disruption. Journal of Entomological Science 34: 210–8 Pfeiffer DG, Killian JC, Rajotte EG, Hull LA, Snow JW. 1991. Mating disruption for reduction of damage of lesser peachtree borer (Lepidoptera: Sesiidae) in Virginia and Pennsylvania peach orchards. Journal of Economic Entomology 84: 218–23 Pierce WC, Nickels CB. 1941. Control of borers on recently top-worked pecan trees. Journal of Economic Entomology 31: 522–6 Pless CD, Stanley WW. 1967. Life history and habits of the dogwood borer, Thamnosphecia scitula (Lepidoptera:Aegeriidae) in Tennessee. Tennessee Agricultural Experiment Station 42: 117–123 Potter DA, Timmons GM. 1981. Factors affecting predisposition of flowering dogwood trees to attack by the dogwood borer. Hortscience 16: 677–9 ——— 1983. Flight phenology of the dogwood borer (Lepidoptera: Sesiidae) and implications for control in Cornus florida L. Journal of Economic Entomology 76: 1069–74 Reed DK, Mikolajczak KL, Krause CR. 1988. Ovipositional behavior of lesser peachtree borer in presence of host-plant volatiles. Journal of Chemical Ecology 14: 237–2 Riedl H, Weires RW, Seaman A, Hoying SA. 1985. Seasonal biology and control of the dogwood borer, Synanthedon scitula (Lepidoptera: Sesiidae) on clonal apple rootstocks in New York. The Canadian Entomologist 117: 1367–77



Volume 135


635

Rocchini LA. 1997. Variation in lodgepole pine susceptibility to pitch moth (Lepidoptera: Sesiidae and Pyralidae) attack at the Prince George tree improvement station. MSc thesis, University of Northern British Columbia, Prince George Rocchini LA, Lindgren BS, RG Bennett. 2000. Effects of resin flow and monoterpene composition on susceptibility of lodgepole pine to attack by the Douglas-fir pitch moth, Syanthedon novaroensis (Lep., Sesiisae). Journal of Applied Entomology 124: 87–92 Rogers LE, Grant JF. 1990. Infestation levels of dogwood borer (Lepidoptera: Sesiidae) larvae on dogwood trees in selected habitats in Tennessee. Journal of Entomological Science 25: 481–5 ——— 1991. Seasonal incidence of male dogwood borer (Lepidoptera: Sesiidae) and other species of clearwing moths in selected habitats in Tennessee. Environmental Entomology 20: 520–5 Rom RC. 1970. Burr knot observations on clonal apple rootstocks in Arkansas. Fruit Varieties Horticultural Digest 24: 66–8 ——— 1973. Burr knot characteristics of six clonal apple rootstocks. Fruit Varieties Journal 27: 84–6 Rom RC, Brown SA. 1979. Factors affecting burr knot formation on clonal Malus rootstocks. Hortscience 14: 231–232 Snow JW, Eichlin TD, Tumlinson JM. 1985. Seasonal captures of clearwing moths (Sesiidae) in traps baited with various formulations of 3,13-octadecadienyl actetate and alcohol. Journal of Agricultural Entomology 2: 73–84 Snow JW, Schwarz M, Klun JA. 1987. The attraction of the grape root borer, Vitacea polistiformis (Harris) (Lepidoptera: Sesiidae), to (E,Z)-2,13-octadecadienyl acetate and the effects of related isomers on attraction. Journal of Entomological Science 4: 371–4 Snow JW, Schwarz M, Eichlin TD. 1989. Captures of clearwing moths (Lepidoptera: Sesiidae) with various octadecadienyl acetates and alcohols in central Georgia during 1983–1985. Environmental Entomology 18: 216–22 Snow JW, Johnson DT, Meyer JR. 1991. The seasonal occurrence of the grape root borer, (Lepidoptera: Sesiidae) in the eastern United States. Journal of Entomological Science 26: 157–68 Suckling DM, Brockerhoff EG. 1999. Control of light brown apple moth (Lepidoptera: Tortricidae) using an attracticide. Journal of Economic Entomology 92: 367–72 Taft WH, Smitley D, Snow JW. 1991. A guide to the clearwing borers (Sesiidae) of the north central United States. Michigan State University, North Central Regional Extension Publication 394 Tumlinson JH. 1979. The chemistry of Sesiidae pheromones. pp 1–10 in Pheromones of the Sesiidae. SEAAR, ARR-NE-6. Washington, District of Columbia: United States Department of Agriculture Tumlinson JH, Yonce CE, Doolittle RE, Heath RR, Gentry CR, Mitchell ER. 1974. Sex pheromones and reproductive isolation of the lesser peachtree borer and the peachtree borer. Science (Washington, DC) 185: 614–6 Underhill GW. 1935. The pecan tree borer in dogwood. Journal of Economic Entomology 28: 393–6 Visser JH. 1986. Host odor perception in phytophagous insects. Annual Review of Entomology 91: 840–4 Wallace PP. 1945. Biology and control of the dogwood borer, Synanthedon scitula Harris. Connecticut Experiment Station Bulletin 488: 373–95 Walton GS. 1986. Association of dogwood borer with the recent decline of dogwood. Journal of Arboriculture 12: 196–8 Warner J, Hay S. 1985. Observations, monitoring, and control of clearwing borers (Lepidoptera: Sesiidae) on apple in central Ontario. The Canadian Entomologist 117: 1471–8 Weires R. 1986. Five years research and experience with control of dogwood borer and related burr knot problems. Compact Fruit Tree 19: 86–9 Williams DB, Witte WT, Hadden CH, Williams HW. 1985. The flowering dogwood in Tennessee. Tennessee Agricultural Extension Service Publication 589 Williams RN, Fickle DS, Grewal PS, Meyer JR. 2002. Assessing the potential of entomopathogenic nematodes to control the grape root borer Vitacea polistiformis (Lepidoptera: Sesiidae) through laboratory and greenhouse bioassays. Biocontrol, Science, and Technology 12: 35–42 Wise JC, Gut LJ. 2002. Trunk sprays for control of dogwood borer, 2000–2001. Arthropod Management Tests 27: A56 Woodside AM. 1952. The apple bark borer. Virginia Agricultural Experiment Station Bulletin 452 Young E, Tyler RH. 1983. Burrknot control on apple. Hortscience 18: 921–2 Zhang A, Linn CE, Wright SE, Prokopy RJ, Reissig WH, Roelofs WL. 1999. Identification of a new blend of apple volatiles attractive to the apple maggot, Rhagoletis pomonella. Journal of Chemical Ecology 25: 1221–31 (Received: 18 October 2002; accepted: 10 June 2003)
